Abstract
Rodents affect soil microbial communities by burrow architecture, diet composition, and foraging behavior. We examined the effect of desert rodents on nitrogen-fixing bacteria (NFB) communities by identifying bacteria colony-forming units (CFU) and measuring nitrogen fixation rates (ARA), denitrification (DA), and CO2 emission in soil from burrows of three gerbil species differing in diets. Psammomys obesus is folivorous, Meriones crassus is omnivorous, consuming green vegetation and seeds, and Dipodillus dasyurus is predominantly granivorous. We also identified NFB in the digestive tract of each rodent species and in Atriplex halimus and Anabasis articulata, dominant plants at the study site. ARA rates of soil from burrows of the rodent species were similar, and substantially lower than control soil, but rates of DA and CO2 emission differed significantly among burrows. Highest rates of DA and CO2 emission were measured in D. dasyurus burrows and lowest in P. obesus. CFU differed among bacteria isolates, which reflected dietary selection. Strains of cellulolytic representatives of the family Myxococcaceae and the genus Cytophaga dominated burrows of P. obesus, while enteric Bacteroides dominated burrows of D. dasyurus. Burrows of M. crassus contained both cellulolytic and enteric bacteria. Using discriminant function analysis, differences were revealed among burrow soils of all rodent species and control soil, and the two axes accounted for 91 % of the variance in bacterial occurrences. Differences in digestive tract bacterial occurrences were found among these rodent species. Bacterial colonies in P. obesus and M. crassus burrows were related to bacteria of A. articulata, the main plant consumed by both species. In contrast, bacteria colonies in the burrow soil of D. dasyurus were related to bacteria in its digestive tract. We concluded that gerbils play an important role as ecosystem engineers within their burrow environment and affect the microbial complex of the nitrogen-fixing organisms in soils.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Ayarbe JP, Kieft TL (2000) Mammal mounds stimulate microbial activity in a semiarid shrubland. Ecology 81:1150–1154
Bar Y, Abramsky Z, Gutterman Y (1984) Diet of gerbilline rodents in Israeli Desert. J Arid Environ 7:371–376
Barua S, Tripathi S, Chakraborty A, Ghosh S, Chakrabarti K (2011) Studies on non-symbiotic diazotrophic bacterial populations of coastal arable saline soils of India. Ind J Microbiol 51:369–376
Belnap J (2002) Nitrogen fixation in biological soil crusts from southeast Utah, USA. Biol Fertil Soils 35:128–135
Belnap J, Büdel B, Lange OL (2001) Biological soil crusts: characteristics and distribution. In: Belnap J, Lange OL (eds) Biological soil crusts: structure, function, and management. Springer, New York
Belov LP, Kostina NV, Naumova EI, Umarov MM (2002) Specific features of nitrogen transformation in the soddy-podsolic soil in the colonies of the common vole Microtus arvalis. Biol Bull 29:88–90
Billings SA, Schaeffer SM, Evans RD (2003) Nitrogen fixation by biological soil crusts and heterotrophic bacteria in an intact Mojave Desert ecosystem with elevated CO2 and added soil carbon. Soil Biol Biochem 35:643–649
Bitton G (2005) Wastewater microbiology. Wiley, Hoboken, New Jersey, USA
Bradbury JF (1970) Isolation and preliminary study of bacteria from plants. Rev Plant Pathol 49:213–218
Bradbury JF (1988) Identification of cultivable bacteria from plants and plant tissue cultures by use of simple classical methods. Acta Hort 225:27–38
Brown JH, Heske EJ (1990) Temporal changes in a Chihuahuan Desert rodent community. Oikos 59:290–302
Ceballos G, Pacheco J, List R (1999) Influence of prairie dogs (Cynomys ludovicianus) on habitat heterogeneity and mammalian diversity in Mexico. J Arid Environ 41:161–172
Contreras LC, Gutierrez JR (1991) Effects of subterranean herbivorous rodent Spalacopus cyanus on the herbaceous vegetation in arid coastal Chile. Oecologia 87:106–109
Daly M, Daly S (1975) Behavior of Psammomys obesus (Rodentia: Gerbillinae) in the Algerian Sahara. Ethology 37:298–321
David KAV, Apte SK, Banerji A, Thomas J (1980) Acetylene reduction assay for nitrogenase activity: gas chromatographic determination of ethylene per sample in less than one minute. Appl Environ Microbiol 39:1078–1080
Davidson AD, Lightfoot DC (2008) Burrowing rodents increase landscape heterogeneity in a desert grassland. J Arid Environ 72:1133–1145
Degen AA, Kam M, Khokhlova IS, Zeevi I (2000) Fiber digestion and energy utilization of fat sand rats (Psammomys obesus) consuming the chenopod Anabasis articulata. Physiol Biochem Zool 73:574–580
Desmet PG, Cowling RM (1999) Patch creation by fossorial rodents: a key process in the revegetation of phytotoxic arid soils. J Arid Environ 43:35–45
Dickman CR (1996) Vagrants in the desert. Nat Aust 25:54–62
Dickman CR (1999) Rodent–ecosystem relationships: a review. In: Singleton G, Hinds L, Leirs H, Zhang Z (eds) Ecologically-based management of rodent pests. Australian Centre for International Agricultural Research, Canberra
Dilworth MJ (1966) Acetylene reduction by nitrogen-fixing preparations from Clostridium pasteurianum. Biochim Biophys Acta 127:285–294
Dobrinskiy LN, Davidov VA, Kryazhimskiy FB, Malafeev Yu M (1983) Small mammals and flora functional linkage in meadow biocenoses (rus). Nauka, Moscow
Drancourt M, Bollet C, Carlioz A, Martelin R, Gayral JP, Raoult D (2000) 16S ribosomal DNA sequence analysis of a large collection of environmental and clinical unidentifiable bacterial isolates. J Clin Microbiol 38:3623–3630
Drury CF, Myrold DD, Beauchamp EG, Reynolds WD (2008) Denitrification techniques for soil. In: Carter MR, Gregovich EG (eds) Soil sampling and methods of analysis. Canadian Society of Soil Science, CRC Press, Taylor & Francis Group, Boca Raton, Florida, USA
Eckford R, Cook FD, Saul D, Aisabie J, Foght J (2002) Free-living heterotrophic nitrogen-fixing bacteria isolated from fuel-contaminated Antarctic soils. Appl Environ Microbiol 68:5181–5185
Eskew DL, Ting IP (1978) Nitrogen fixation by legumes and blue-green algae-lichen crusts in a Colorado desert environment. Amer J Bot 65:850–856
Evans RD, Belnap J (1999) Long-term consequences of disturbance on nitrogen dynamics in arid ecosystem. Ecology 80:150–160
Fichet-Calvet E, Jomaa I, Giraudoux P, Ashford RW (1999) Estimation of fat sand rat Psammomys obesus abundance by using surface indices. Acta Theriol 44:353–362
Formozov NA, Kizilova AK, Panteleeva AN, Naumova EI (2012) Nitrogen fixation as a possible physiological basis of coprophagy in pikas (Ochotona, Lagomorpha, Mammalia). Doklady Akad Nauk 443:126–129
Gallardo A, Schlesinger WH (1992) Carbon and nitrogen limitations of soil microbial biomass in desert ecosystems. Biogeochemistry 18:1–17
Garcia-Amado MA, Godoy-Vitorino F, Piceno YM, Tom LM, Andersen GL, Herrera EA, Dominguez-Bello MG (2012) Bacterial diversity in the cecum of the world’s largest living rodent (Hydrochoerus hydrochaeris). Microb Ecol 63:719–725
Gardini F, Atisari LV, Guerzony ME, Sequi P (1991) A simple gas chromatographic approach to evaluate CO2 release, N2O evolution, and O2 uptake from soil. Biol Fertil Soils 12:1–4
Grant WE, McBayer JF (1981) Effects of mound formation by pocket gophers (Geomys bursarius) on old-field ecosystems. Pedobiologia 22:21–28
Greene RA, Reynard C (1932) The influence of two burrowing rodents, Dipodomys spectabilis spectabilis (kangaroo rat) and Neotoma albigula albigula (pack rat) on desert soils in Arizona. Ecology 13:73–80
Groffman PM, Holland EA, Myrold DD, Robertson GP, Zou X (1999) Denitrification. In: Robertson GP, Coleman DC, Bledsoe CS, Sollins P (eds) Standard soil methods for long-term ecological research. Oxford University Press, New York, New York, USA
Gromov VS (2001) Daytime activities and social interactions in a colony of the fat sand rats, Psammomys obesus, at the Negev Highlands, Israel. Mammalia 65:13–28
Gromov VS, Krasnov BR, Shenbrot GI (2001) Behavioural correlates of spatial distribution in Wagner’s gerbil Gerbillus dasyurus (Rodentia, Gerbillinae). Mammalia 65:111–120
Gutierrez JR, Meserve PL, Herrera S, Contreras LC, Jaksic FM (1997) Effects of small mammals and vertebrate predators on vegetation in the Chilean semiarid zone. Oecologia 109:398–406
Hara S, Hashidoko Y, Desyatkin RV, Hatano R, Tahara S (2009) High rate of N2 fixation by East Siberian cryophilic soil bacteria as determined by measuring acetylene reduction in nitrogen-poor medium solidified with gellan gum. Appl Environ Microbiol 75:2811–2819
Hardy RWF, Burns RD, Holsten RD (1973) Applications of the acetylene–ethylene assay for measurement of nitrogen fixation. Soil Biol Biochem 5:59–72
Harrison DL, Bates JJ (1991) The mammals of Arabia, 2nd edn. Harrison Zoological Museum, Kent
Hatough-Bouran A (1990) The burrowing habits of desertic rodents Jaculus jaculus and Gerbillus dasyurus in the Shaumari Reserve in Jordan. Mammalia 54:341–359
Hawkins LK (1996) Burrows of kangaroo rats are hotspots for desert soil fungi. J Arid Environ 32:239–249
Herrera J, Kramer CL, Reichman OJ (1999) Microfungal community changes in rodent food stores over space and time. Microb Ecol 38:79–91
Heske EJ, Brown JH, Guo Q (1993) Effect of kangaroo rat exclusion on vegetation structure and plant species diversity in the Chihuahuan Desert. Oecologia 95:520–524
Hobbs RJ, Hobbs VJ (1987) Gophers and grassland: a model of vegetation response to patchy soil disturbance. Vegetation 69:141–146
Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology. Williams and Wilkins, Baltimore
Inouye RS, Huntly NJ, Tilman D, Tester JR (1987) Pocket gophers (Geomys bursarius), vegetation, and soil nitrogen along a successional sere in east central Minnesota. Oecologia 72:178–184
Inouye RS, Huntly NJ, Wasley GA (1997) Effects of pocket gophers (Geomys bursarius) on microtopographic variation. J Mammal 78:1144–1148
Jensen HL (1941) Nitrogen fixation and cellulose degradation by soil micro-organisms. Proc Linn Soc NSW 66:239–249
Jones JB Jr (1991) Kjeldahl method for nitrogen determination. Micro–Macro Publishing, Athens
Jones CG, Lawton GH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386
Kam M, Degen AA (1988) Water, electrolyte and nitrogen balances of fat sand rat (Psammomys obesus) when consuming the saltbush Atriplex halimus. J Zool 215:453–462
Kam M, Khokhlova IS, Degen AA (1997) Granivory and plant selection by desert gerbils of different body size. Ecology 78:2218–2229
Kiviat E (1978) Vertebrate use of muskrat lodges and burrows. Estuaries 1:196–200
Klein DA (1977) Seasonal carbon flow and decomposer parameter relationships in a semiarid grassland soil. Ecology 58:184–190
Knowles R, Neufeld R, Simpson S (1974) Acetylene reduction (nitrogen fixation) by pulp and paper mill effluents and by Klebsiella isolates from effluents and environmental conditions. Appl Microbiol 28:608–613
Krasnov BR, Shenbrot GI, Khokhlova IS, Degen AA, Rogovin KA (1996) On the biology of Sundevall’s jird (Meriones crassus Sundevall, 1842) (Rodentia: Gerbillidae) in the Negev Highlands, Israel. Mammalia 60:375–391
Kuznetsova TA, Kostina NV, Naumova EI, Umarov MM (2010) Microbial nitrogen fixation in the gastrointestinal tract of Kalmykia gerbils (Meriones tamariscinus and Meriones meridianus). Biol Bull 37:476–479
Kuznetsova TA, Roshchina ES, Kostina NV, Umarov MM (2006) Soil biological activity in the Chernye Zemli, Kalmykia, inhabited by gerbils Meriones tamariscinus and M. meridianus. Biol Bull 33:92–99
Li CY, Maser C, Maser Z, Caldwell BA (1986) Role of three rodents in forest nitrogen fixation in western Oregon: another aspect of mammal-mycorrhizal fungus-tree mutualism. West N Am Nat 46:411–414
Lin YT, Huang YJ, Tang SL, Whitman WB, Coleman DC, Chiu CY (2010) Bacterial community diversity in undisturbed perhumid montane forest soils in Taiwan. Microb Ecol 59:369–378
Lysak LV, Dobrovolskaya TG, Skvortsova IN (2003) Methods of soil microbial diversity estimation and soil bacteria identification (rus). Max-press, Moscow
Malizia AI, Kittlein MJ, Busch C (2000) Influence of the subterranean herbivorous rodent Ctenomys talarum on vegetation and soil. Int J Mammal Biol 65:172–182
Manaeva ES, Naumova EI, Kostina NV, Umarov MM, Dobrovol’skaya TG (2012) Functional features of microbial communities in the digestive tract of field voles (Microtus rossiaemeridionalis and Clethrionomys glareolus). Biol Bull 39:346–350
Meshcherskii IG, Naumova EI, Kostina NV, Varshavskii AA, Umarov MM, Yur’eva OS (2004) Effect of deficiency of dietary nitrogen on cellulose digestibility and nitrogen fixing flora activity in sibling vole Microtus rossiaemeridionalis. Izv Akad Nauk Ser Biol 5:556–560
Moorhead DL, Fisher FM, Whitford WG (1988) Cover of spring annuals on nitrogen-rich kangaroo rat mounds in a Chihuahuan desert grassland. Am Midl Nat 120:443–447
Mun HT, Whitford WG (1990) Factors affecting annual plants assemblages on banner-tailed kangaroo rat mounds. J Arid Environ 18:165–173
Naumova EI, Ushakova NA, Meshcherskii IG, Kostina NV, Umarov MM (2000) Nitrogen fixation: a new phenomenon in rodent nutrition. Izv Akad Nauk Ser Biol 3:329–331
Newbould P (1989) Nitrogen factor in organic matter cycling and utilisation in arid soils. Arid Soil Res Rehabil 3:295–313
Persson T (1983) Influence of soil animals on nitrogen mineralisation in a northern Scots pine forest. In: Lebrun P, Andre HM, de Medts A, Gregoire-Wibo C (eds) New trends in soil biology: Proceedings of the 8th International Colloquium of Soil Zoology. Dieu-Brichart, Louvain-la-Neuve
Polyanskaya LM, Zvyagintsev DG (1995) Microbial succession in soil. Physiol Gen Biol Rev 9:1–68
Postgate J (1998) Nitrogen fixation. Cambridge University Press, Cambridge, United Kingdom
Reichman OJ, Seabloom EW (2002) The role of pocket gophers as subterranean ecosystem engineers. Trends Ecol Evol 17:44–49
Rice WA (1979) Influence of the nitrogen content of straw amendments on nitrogenase activity in waterlogged soil. Soil Biol Biochem 11:187–191
Roper MM, Ladha JK (1995) Biological N2 fixation by heterotrophic bacteria in association with straw. Plant Soil 174:211–224
Rychert R, Skujins J (1974) Nitrogen fixation by blue-green algae-lichen crust in the Great Basin Desert. Soil Sci Soc Am J 38:768–771
Samson DA, Philippi TE, Davidson DW (1992) Granivory and competition as determinants of annual plant diversity in the Chihuahuan Desert. Oikos 65:61–80
Shenbrot G, Krasnov B, Burdelov S (2010) Long-term study of population dynamics and habitat selection of rodents in the Negev Desert. J Mammal 91:776–786
Shenbrot G, Krasnov BR, Khokhlova I, Demidova T, Fielden L (2002) Habitat-dependent differences in architecture and microclimate of the burrows of Sundevall’s jird (Meriones crassus) (Rodentia: Gerbillinae) in the Negev Desert, Israel. J Arid Environ 51:265–279
Sheppard SC, Addison JA (2008) Soil sample handling and storage. In: Carter MR, Gregovich EG (eds) Soil sampling and methods of analysis. Canadian Society of Soil Science, CRC Press, Taylor & Francis Group, Boca Raton, Florida, USA
Skinner JD, Smithers RH (1990) The mammals of the southern African subregion. University of Pretoria, Pretoria
Spencer SR, Cameron G, Eshelman BD, Cooper LC, Williams LR (1985) Influence of pocket gopher mounds on a Texas coastal prairie. Oecologia 66:111–115
Stacey G, Burris RH, Evans HJ (1992) Biological nitrogen fixation. Chapman and Hall Inc, Routledge
Tchabovsky AV, Krasnov BR (2002) Spatial distribution of Psammomys obesus (Rodentia: Gerbillinae) in relation to vegetation in the Negev desert of Israel. Mammalia 66:361–368
Tchabovsky AV, Krasnov BR, Khokhlova IS, Shenbrot GI (2001) The effect of vegetation cover on vigilance and foraging tactics in the fat sand rat Psammomys obesus. J Ethol 19:105–113
Van Toan Pham (2006) Non-symbiotic nitrogen fixers. In: Van Toan Pham (ed) Bioertilizer manual. Bioertilizer Project, Forum for Nuclear Cooperation in Asia (FNCA), Japan Atomic Industrial Forum (JAIF), Tokyo, Japan
Varshavskii AA, Puzachenko AY, Naumova EI, Kostina NV (2003) The enzymatic activity of the gastrointestinal tract microflora of the greater mole rat (Spalax microphtalmus, Spalacidae, Rodentia). Doklady biological sciences: proceedings of the Academy of Sciences of the USSR. Biol Sci Sect 392:439–441
Vecherskii M, Naumova E, Kostina N, Umarov M (2009) Assimilation of biological nitrogen by European beaver. Biol Bull Russ Acad Sci 36:92–95
Verhoef HA, Prast JE, Verweij RA (1988) Relative importance of fungi and algae in the diet and nitrogen nutrition of Orchesella cincta and Tomocerus minor (Collembola). Funct Ecol 2:195–201
Villareal D, Clark KL, Branch LC, Hierro JL, Machicote M (2008) Alteration of ecosystem structure by a burrowing herbivore, the plains vizcacha (Lagostomus maximus). J Mammal 89:700–711
West NE (1991) Nutrient cycling in soils of semiarid and arid regions. In: Skujins J (ed) Semiarid lands and deserts: soil resource and reclamation. Marcel Dekker, New York
Whitford WG (1993) Animal feedbacks in desertification: an overview. Rev Chil Hist Nat 66:243–251
Yom-Tov Y (1991) Character displacement in the psammophile Gerbillidae of Israel. Oikos 60:173–179
Yoshinari T, Hynes R, Knoudes R (1977) Acetylene inhibition of nitrous oxide reduction and measurement of denitrification and nitrogen fixation in soil. Soil Biol Biochem 9:177–183
Zaady E, Groffman P, Shachak M (1998) Nitrogen fixation in macro and microphytic patches in the Negev Desert. Soil Biol Biochem 30:449–454
Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 5:539–554
Zenova GM, Stepanov AL, Likhacheva AA, Manucharova NA (2002) Practice works on soil biology. MSU Publishing, Moscow (in Russian)
Zhang YM, Liu JK, Du YR (2004) The impact of plateau zokor Myospalax fontanierii burrows on alpine meadow vegetation on the Qinghai-Xizang (Tibetan) plateau. Acta Theriol 49:43–51
Zhang YM, Zhang ZB, Liu JK (2003) Burrowing rodents as ecosystem engineers: the ecology and management of plateau zokors Myospalax fontanierii in alpine meadow ecosystems on the Tibetan Plateau. Mammal Rev 33:284–294
Acknowledgments
We thank two anonymous reviewers for their helpful comments. The access and research at our study site was conducted under permit number 2003/16737 from the Israel Nature and National Parks Protection Authority (INNPPA). This permit included permission for trappings of rodent species. This is publication no. 810 of the Mitrani Department of Desert Ecology.
Conflict of Interest
The authors declare that they have no conflict of interests.
Author information
Authors and Affiliations
Corresponding author
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 78.5 kb)
Rights and permissions
About this article
Cite this article
Kuznetsova, T.A., Kam, M., Khokhlova, I.S. et al. Desert Gerbils Affect Bacterial Composition of Soil. Microb Ecol 66, 940–949 (2013). https://doi.org/10.1007/s00248-013-0263-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-013-0263-7