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Journal of Arid Land  2020, Vol. 12 Issue (3): 508-521    DOI: 10.1007/s40333-020-0015-8
Research article     
Effects of rodent-induced disturbance on eco-physiological traits of Haloxylon ammodendron in the Gurbantunggut Desert, Xinjiang, China
XIANG Yanling1, WANG Zhongke1, LYU Xinhua1, HE Yaling2, LI Yuxia1, ZHUANG Li1, ZHAO Wenqin1,*()
1 College of Life Sciences, Shihezi University, Shihezi 832003, China
2 School of Medicine, Shihezi University, Shihezi 832003, China
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Disturbance by rodents alters the morphologies and nutrients of plants as well as the physical-chemical properties of the soils. Changes in plants are considered to be mechanisms of defense against the disturbance by rodents. Rodents gnaw on the assimilating branches of Haloxylon ammodendron (CA Mey.) Bunge and burrow under the bushes in the desert ecosystems of Xinjiang, China. However, eco-physiological responses of different age groups of H. ammodendron to the disturbance by rodents are not well understood. In this study, soil physical-chemical properties under the shrubs and the above-ground morphological, physiological and biochemical features of assimilating branches of H. ammodendron of different age groups (i.e., young, 30-100 cm; middle-aged, 100-200 cm; and mature, >200 cm) in burrowed and non-burrowed (control) areas were studied in 2018. We found that disturbance by rodents significantly increased the crown width and total branching rates of young and middle-aged H. ammodendron. Photosynthetic pigment contents of assimilating branches of H. ammodendron were significantly reduced under the disturbance by rodents. In term of plant nutrients, the main differences among different age groups of H. ammodendron under the disturbance by rodents occurred in the total soluble sugar and reducing sugar contents that decreased in young plants, increased in middle-aged plants, and did not affect in mature plants. Crude protein and phosphorus contents significantly increased, while crude fiber and calcium contents significantly decreased in young plants. Crude fat and calcium contents significantly decreased in middle-aged plants. Soil organic matter (SOM), total nitrogen (TN), available nitrogen (AN) and available potassium (AK) contents in the topsoil (0-20 cm), which are conducive to forming ''fertile islands'', also increased under the disturbance by rodents. In particular, soil AN and AK were the major factors affecting the above-ground morphological characteristics of H. ammodendron in burrowed areas. Overall, the response and defense strategies of H. ammodendron to the disturbance by rodents differed among different age groups, and the effect of the disturbance by rodents on H. ammodendron gradually weakened with the increasing plant age.

Key wordsage groups      morphology      assimilating branches      soil physical-chemical properties      photosynthetic pigments     
Received: 01 June 2019      Published: 10 May 2020
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About author: *Corresponding author: ZHAO Wenqin (E-mail:
Cite this article:

XIANG Yanling, WANG Zhongke, LYU Xinhua, HE Yaling, LI Yuxia, ZHUANG Li, ZHAO Wenqin. Effects of rodent-induced disturbance on eco-physiological traits of Haloxylon ammodendron in the Gurbantunggut Desert, Xinjiang, China. Journal of Arid Land, 2020, 12(3): 508-521.

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Fig. 1 Difference in above-ground morphological characteristic (a-d) of H. ammodendron with different ages (heights) in burrowed and control areas. Boxes represent the interquartile range (containing 50% of values), lines across boxes represent medians, whiskers indicate the highest and lowest values, and circle indicates outlier. * and ** indicate signi?cant differences between burrowed and control areas at P<0.05 and P<0.01 levels, respectively. (e), Correlation between height and basal stem of H. ammodendron in burrowed (R2) and control (R02) areas; and (f) correlation between height and crown width of H. ammodendron in burrowed (R2) and control (R02) areas.
Fig. 2 Difference of nutrient content in assimilating branches of H. ammodendron in burrowed and control areas. Bars represent standard error. * and ** indicate signi?cant differences between burrowed and control areas at P<0.05 and P<0.01 levels, respectively.
Fig. 3 Comparison of photosynthetic pigment content of H. ammodendron in burrowed and control areas. Different lowercase letters represent signi?cant differences among different age groups (heights) of H. ammodendron at P<0.05 level. * and ** indicate signi?cant differences between burrowed and control areas at P<0.05 and P<0.01 levels, respectively.
Fig. 4 Difference in soil physical-chemical property of H. ammodendron in burrowed and control areas. Different lowercase letters indicate significant difference among different soil depths at P<0.05 level. Boxes represent the interquartile range (containing 50% of values), lines across boxes represent medians, whiskers indicate the highest and lowest values, and circle indicates outlier. * and ** indicate signi?cant differences between burrowed and control areas at P<0.05 and P<0.01 levels, respectively. SOM, soil organic matter; TN, total nitrogen; TP, total phosphorus; TK, total potassium; AN, available nitrogen; AP, available phosphorus; AK, available potassium.
Fig. 5 Correlation between physical-chemical property of topsoil and above-ground morphology of H. ammodendron, as determined by redundancy analysis (RDA). (a), burrowed areas; and (b), control areas. △, young H. ammodendron; ○, middle-aged H. ammodendron; □, mature H. ammodendron; SOM, soil organic matter; TN, total nitrogen; TP, total phosphorus; TK, total potassium; AN, available nitrogen; AP, available phosphorus; AK, available potassium.
Sample plot Soil variable Eigenvalues Explained variance (%) F P
Burrowed area AN 0.505 50.5 25.5 0.002
AK 0.309 30.9 11.2 0.002
TP 0.107 10.7 3.0 0.072
TK 0.078 7.8 2.1 0.122
SOM 0.045 4.5 1.2 0.270
pH 0.038 3.8 1.0 0.354
AP 0.018 1.8 0.5 0.578
TN 0.014 1.4 0.3 0.690
Control area AN 0.426 42.6 18.5 0.002
AK 0.305 30.5 11.0 0.004
TN 0.270 27.0 9.2 0.012
AP 0.256 25.6 8.6 0.008
SOM 0.101 10.1 2.8 0.104
TP 0.041 4.1 1.1 0.294
pH 0.008 0.8 0.2 0.762
TK 0.002 0.2 <0.1 0.878
Table 1 Forward selection of soil variables during the redundancy analysis
Fig. S1 Pearson′s correlation coefficient among physiological indices of assimilating branches of H. ammodendron in burrowed and control areas. * and ** indicate signi?cant differences between these indices at P<0.05 and P<0.01 levels, respectively. TSS, total soluble sugar; RS, reducing sugar; CF, crude fiber; EE, crude fat; CP, crude protein; P, phosphorous; Ca, calcium; Cha, Chlorophyll a; Chb, Chlorophyll b; Car, carotenoid; Total Chl, total chlorophyll.
TSS 0.58 -0.32 -0.55 -0.21 -0.35 0.50 -0.46
RS 0.55 -0.38 -0.52 -0.17 -0.40 0.35 -0.29
CF 0.06 -0.47 0.03 0.26 -0.35 -0.06 0.34
EE -0.38 -0.82** 0.12 -0.30 -0.79* -0.43 -0.31
CP -0.11 0.62* 0.70* 0.15 0.75* 0.18 0.78*
P 0.03 0.61 0.54 0.11 0.78* 0.71* 0.40
Ca 0.14 -0.74* -0.54 -0.43 -0.88** -0.31 -0.82**
Table S1 Correlation of nutrient between topsoil and assimilating branches of H. ammodendron in burrowed area
[1]   Allington G R H, Valone T J.2014. Islands of fertility: A byproduct of grazing? Ecosystems, 17(1): 127-141.
[2]   Andino N, Borghi C E.2018. Occurrence of ctenomys mendocinus in a high-altitude cold desert: Effect on density, biomass, and fitness of sagebrush plants. Arctic, Antarctic, and Alpine Research, 49(1): 53-60.
[3]   Bao S D.1999. Methods of Agrochemical Soil Analysis. Beijing: China Agriculture Press, 25-35. (in Chinese)
[4]   Barthelemy H, Stark S, Michelsen A, et al.2018. Urine is an important nitrogen source for plants irrespective of vegetation composition in an Arctic tundra: Insights from a 15N-enriched urea tracer experiment. Journal of Ecology, 106(1): 367-378.
[5]   Barton K E, Koricheva J.2010. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. American Naturalist, 175(4): 481-493.
[6]   Barton K E.2016. Low tolerance to simulated herbivory in Hawaiian seedlings despite induced changes in photosynthesis and biomass allocation. Annals of Botany, 117(6): 1053-1062.
[7]   Berke S K.2010. Functional groups of ecosystem engineers: a proposed classification with comments on current issues. Integrative & Comparative Biology, 50(2): 147-157.
[8]   Braak C J F T, Prentice I C.2004. A theory of gradient analysis. Advances in Ecological Research, 34: 23-28.
[9]   Campos-Vargas R, Saltveit M E.2010. Involvement of putative chemical wound signals in the induction of phenolic metabolism in wounded lettuce. Physiologia Plantarum, 114(1): 73-84.
[10]   Christie K S, Ruess R W, Lindberg M S, et al.2014. Herbivores influence the growth, reproduction, and morphology of a widespread arctic willow. PloS ONE, 9(7): e101716.
[11]   Dong B C, Fu T, Luo F L, et al.2017. Herbivory-induced maternal effects on growth and defense traits in the clonal species Alternanthera philoxeroides. Science of the Total Environment, 605-606: 114-123.
[12]   Ewing S A, Southard R J, Macalady J L, et al.2007. Soil microbial fingerprints, carbon, and nitrogen in a Mojave Desert creosote-bush ecosystem. Soil Science Society of America Journal, 71(2): 469-475.
[13]   Falkenberg J C, Clarke J A.1998. Microhabitat use of deer mice: Effects of interspecific interaction risks. Journal of Mammalogy, 79(2): 558-565.
[14]   Hagenah N, Bennett N C.2013. Mole rats act as ecosystem engineers within a biodiversity hotspot, the Cape Fynbos. Journal of Zoology, 289(1): 19-26.
[15]   Hakes A S, Cronin J T.2011. Resistance and tolerance to herbivory in Solidago altissima (Asteraceae): Genetic variability, costs, and selection for multiple traits. American Journal of Botany, 98(9): 1446-1455.
[16]   He A L, Niu S Q, Zhao Q, et al.2018. Induced salt tolerance of perennial ryegrass by a novel bacterium strain from the rhizosphere of a desert shrub Haloxylon ammodendron. International Journal of Molecular Sciences, 19(2): 469.
[17]   Huang G, Cao Y F, Wang B, et al.2015. Effects of nitrogen addition on soil microbes and their implications for soil Cemission in the Gurbantunggut Desert, center of the Eurasian Continent. Science of the Total Environment, 515-516: 215-224.
[18]   Jiang H P, Wu N, Yang W K.2007. Effects of Rhombomys opimus on microbial quantity, soil moisture content and soil nutrient content in a desert. Arid Zone Research, 24(2): 187-192. (in Chinese)
[19]   Jung S.2004. Effect of chlorophyll reduction in Arabidopsis thaliana by methyl jasmonate or norflurazon on antioxidant systems. Plant Physiology & Biochemistry (Paris), 42(3): 225-231.
[20]   Kafle D, Wurst S.2019. Legacy effects of herbivory enhance performance and resistance of progeny plants. Journal of Ecology, 107(1): 58-68.
[21]   Kang J J, Zhao W, Ying Z, et al.2017. Calcium chloride improves photosynthesis and water status in the C4 succulent xerophyte Haloxylon ammodendron under water deficit. Plant Growth Regulation, 82(3): 467-478.
doi: 10.1007/s10725-017-0273-4
[22]   Karasov T, Chae E, Herman J, et al.2017. Mechanisms to mitigate the tradeoff between growth and defense. Plant and Cell, 29(4): 666-680.
doi: 10.1105/tpc.16.00931
[23]   Kindler D S, Robert S.1970. Nutrients and the reaction of two alfalfa clones to the spotted alfalfa aphid. Journal of Economic Entomology, 63(3): 938-940.
[24]   Koch K E.1996. Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 47(1): 509-540.
doi: 10.1146/annurev.arplant.47.1.509
[25]   Kozlov M V, Zvereva E L.2012. Delayed local responses of downy birch to damage by leafminers and leafrollers. Oikos, 121(3): 428-434.
doi: 10.1111/j.1600-0706.2011.19625.x
[26]   Lacey E A, Patton J L, Cameron G N, et al.2001. Community Ecology of Subterranean Rodents. Chicago: University of Chicago Press, 75-76.
[27]   Lepš J, Šmilauer P.2003. Multivariate analysis of ecological data using CANOCO. Cambridge: Cambridge University Press, 60-65.
[28]   Li C J, Li Y, Ma J.2011. Spatial heterogeneity of soil chemical properties at fine scales induced by Haloxylon ammodendron (Chenopodiaceae) plants in a sandy desert. Ecological Research, 26(2): 385-394.
doi: 10.1007/s11284-010-0793-0
[29]   Li L, Li H X, Zeng H L, et al.2016. Exogenous jasmonic acid and cytokinin antagonistically regulate rice flag leaf senescence by mediating chlorophyll degradation, membrane deterioration, and senescence-associated genes expression. Journal of Plant Growth Regulation, 35(2): 366-376.
doi: 10.1007/s00344-015-9539-0
[30]   Lichtenthaler H K.1987. Chlorolshylls and carotenoids: Pigments of photosynthetic biomembranes. Methods in Enzymology, 148: 350-382.
[31]   Liu W, Xu W X, Yang W K, et al.2012. Food habits of the great gerbil (Rhombomys opimus) in the Southern Gurbantunggut Desert, Xinjiang, China. Pakistan Journal of Zoology, 44(4): 931-936.
[32]   Luo Q, Chen Q, Ning H, et al.2017. Chronosequence-based population structure and natural regeneration of Haloxylon ammodendron plantation in the southern edge of the Gurbantunggut Desert, Northwestern China. Russian Journal of Ecology, 48(4): 364-371.
doi: 10.1134/S1067413617040130
[33]   Ma T, Zheng J H, Wen A M, et al.2018. Group coverage of burrow entrances and distribution characteristics of desert forest-dwelling Rhombomys opimus based on unmanned aerial vehicle (UAV) low-altitude remote sensing: A case study at the southern margin of the Gurbantunggut Desert in Xinjiang. Acta Ecologica Sinica, 38(3): 953-963. (in Chinese)
[34]   Mabry T J, Hunziker J H, Difeo D R J.1977. Creosote bush: Biology and chemistry of Larrea in new world deserts. Desert Plants, 31(5): 399.
[35]   Mao L Z, Lu H F, Wang Q, et al.2007. Comparative photosynthesis characteristics of Calycanthus chinensis and Chimonanthus praecox. Photosynthetica, 45(4): 601-605.
doi: 10.1007/s11099-007-0103-4
[36]   Mares M A, Ojeda R A, Borghi C E, et al.1997. How desert rodents overcome halophytic plant defenses. Bioscience, 47(10): 699-704.
doi: 10.2307/1313210
[37]   Munns R, Tester M.2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology, 59(1): 651-681.
doi: 10.1146/annurev.arplant.59.032607.092911
[38]   Nabity P D, Zavala J A, DeLucia E H.2013. Herbivore induction of jasmonic acid and chemical defences reduce photosynthesis in Nicotiana attenuata. Journal of Experimental Botany, 64(2): 685-694.
doi: 10.1093/jxb/ers364
[39]   Nelson N.1944. A photometric adaptation of the Somogyi method for determination of glucose. Journal of Biological Chemistry, 153: 375-380.
[40]   Ngatia L W, Turner B L, Njoka J T, et al.2015. The effects of herbivory and nutrients on plant biomass and carbon storage in vertisols of an East African savanna. Agriculture Ecosystems & Environment, 208: 55-63.
[41]   O'Reilly-Wapstra J M, Potts B M, McArthur C, et al.2005. Inheritance of resistance to mammalian herbivores and of plant defensive chemistry in a Eucalyptus species. Journal of Chemical Ecology, 31(3): 519-537.
doi: 10.1007/s10886-005-2030-9
[42]   Roe J H.1955. The determination of sugar in blood and spinal fluidwith anthrone reagent. Journal of Biological Chemistry, 212(1): 335-343.
[43]   Rogovin K, Randall J A, Kolosova I, et al.2003. Social correlates of stress in adult males of the great gerbil, Rhombomys opimus, in years of high and low population densities. Hormones & Behavior, 43(1): 132-139.
[44]   Schweissing F C, Wilde G.1979. Temperature and plant nutrient effects on resistance of seedling sorghum to the greenhug. Journal of Economic Entomology, 72(1): 20-23.
doi: 10.1093/jee/72.1.20
[45]   Shimizu-Sato S, Tanaka M, Mori H.2009. Auxin-cytokinin interactions in the control of shoot branching. Plant Molecular Biology, 69(4): 429-435.
doi: 10.1007/s11103-008-9416-3
[46]   Siemens D H, Garner S H, Mitchell-Olds T, et al.2002. Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology, 83(2): 505-517.
doi: 10.1890/0012-9658(2002)083[0505:CODITC]2.0.CO;2
[47]   Sitters J, te Beest M, Cherif M, et al.2017. Interactive effects between reindeer and habitat fertility drive soil nutrient availabilities in arctic tundra. Ecosystems, 20(7): 1266-1277.
doi: 10.1007/s10021-017-0108-1
[48]   Sivritepe N, Kumral N A, Erturk U, et al.2009. Responses of grapevines to two-spotted spider mite mediated biotic stress. Journal of Biological Sciences, 9(4): 311-318.
doi: 10.3923/jbs.2009.311.318
[49]   Somogyi M.1952. Note on sugar determination. Journal of Biological Chemistry, 195(1): 19-23.
[50]   Sotelo P, Pérez E, Najar-Rodriguez A, et al.2014. Brassica plant responses to mild herbivore stress elicited by two specialist insects from different feeding guilds. Journal of Chemical Ecology, 40(2): 136-149.
doi: 10.1007/s10886-014-0386-4
[51]   Steingraeber D A, Waller D M.1986. Non-stationarity of tree branching patterns and bifurcation ratios. Series B, Biological Sciences, 228(1251): 187-194.
[52]   Tchabovsky A V, Krasnov B, Khokhlova I S, et al.2001. The effect of vegetation cover on vigilance and foraging tactics in the fat sand rat Psammomys obesus. Journal of Ethology, 19(2): 105-113.
doi: 10.1007/s101640170006
[53]   Ulappa A C, Kelsey R G, Frye G G, et al.2014. Plant protein and secondary metabolites influence diet selection in a mammalian specialist herbivore. Journal of Mammalogy, 95(4): 834-842.
doi: 10.1644/14-MAMM-A-025
[54]   Whitford W G, Kay F R.1999. Biopedturbation by mammals in deserts: a review. Journal of Arid Environments, 41(2): 203-230.
doi: 10.1006/jare.1998.0482
[55]   Whitney G G.1976. The bifurcation ratio as an indicator of adaptive strategy in woody plant species. Bulletin of the Torrey Botanical Club, 103(2): 67-72.
doi: 10.2307/2484833
[56]   Xu M H, Liu T, Jiang L.2012. Study on the harm characteristics of rodents to Haloxylon ammodendrom and its control for ecological threshold value in the south of Gurbantonggut Desert. Journal of Arid Land Resources and Environment, 26(6): 126-133. (in Chinese)
[57]   Xu W X, Liu W, Yang W K, et al.2012. Rhombomys opimus contribution to the ''fertile island'' effect of tamarisk mounds in Junggar Basin. Ecological Research, 27(4): 775-781.
doi: 10.1007/s11284-012-0952-6
[58]   Zhang K, Su Y Z, Liu T N, et al.2016. Leaf C:N:P stoichiometrical and morphological traits of Haloxylon ammodendron over plantation age sequences in an oasis-desert ecotone in North China. Ecological Research, 31(3): 449-457.
doi: 10.1007/s11284-016-1353-z
[59]   Zhang S L, Kou M J, Bing J C, et al.2001. Investigation of forest rodents fauna in Gansu province. Forest Pest and Disease, 6: 26-28. (in Chinese)
[60]   Zhang S L, Chen Y W, Ma J M, et al.2009. Effect of the damage and feeding of Rhombimys opimus on the growth of Haloxylon ammodendron. Forest Pest & Disease, 28(1): 7-9. (in Chinese)
[61]   Züst T, Rasmann S, Agrawal A A.2015. Growth-defense tradeoffs for two major anti-herbivore traits of the common milkweed Asclepias syriaca. Oikos, 124(10): 1404-1415.
doi: 10.1111/oik.2015.v124.i10
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