Advertisement

Subterranean Desert Rodents (Genus Ctenomys) Create Soil Patches Enriched in Root Endophytic Fungal Propagules

  • Victoria Miranda
  • Carolina Rothen
  • Natalia Yela
  • Adriana Aranda-Rickert
  • Johana Barros
  • Javier Calcagno
  • Sebastián Fracchia
Soil Microbiology

Abstract

Subterranean rodents are considered major soil engineers, as they can locally modify soil properties by their burrowing activities. In this study, the effect of a subterranean rodent of the genus Ctenomys on soil properties and root endophytic fungal propagules in a shrub desert of northwest Argentina was examined. Our main goal was to include among root endophytic fungi not only arbuscular mycorrhiza but also the dark septate endophytes. We compared the abundance of fungal propagules as well as several microbiological and physicochemical parameters between soils from burrows and those from the surrounding landscape. Our results show that food haulage, the deposition of excretions, and soil mixing by rodents’ burrowing promote soil patchiness by (1) the enrichment in both types of root endophytic fungal propagules; (2) the increase in organic matter and nutrients; and (3) changes in soil edaphic properties including moisture, field capacity, and texture. These patches may play a critical role as a source of soil heterogeneity in desert ecosystems, where burrows constructed in interpatches of bare soil can act, once abandoned, as “islands of fertility,” promoting the establishment of plants in an otherwise hostile environment.

Keywords

Biopedturbation Fungal dispersion Dark septate endophytes Arbuscular mycorrhiza Monte Desert 

Notes

Funding Information

This research was supported by Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET-PICT 0546).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2018_1227_MOESM1_ESM.docx (14 kb)
ESM 1 (DOCX 13 kb)

References

  1. 1.
    Darwin C (1881) The formation of vegetable mould through the action of worms, with observations on their habits. J. Murray, LondonCrossRefGoogle Scholar
  2. 2.
    Bardgett R (2010) The biology of soil: a community and ecosystem approachGoogle Scholar
  3. 3.
    Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189.  https://doi.org/10.3114/sim.53.1.173 CrossRefGoogle Scholar
  4. 4.
    Smith SE, Read DJ (2008) Mycorrhizal symbiosis 3rd edn. Academic Press, San Diego, p 787Google Scholar
  5. 5.
    Jumpponen A (2001) Dark septate endophytes—are they mycorrhizal? Mycorrhiza 11:207–211.  https://doi.org/10.1007/s005720100112 CrossRefGoogle Scholar
  6. 6.
    Wu Y, Liu T, He X (2009) Mycorrhizal and dark septate endophytic fungi under the canopies of desert plants in Mu Us Sandy Land of China. Front Agric China 3:164–170.  https://doi.org/10.1007/s11703-009-0026-x CrossRefGoogle Scholar
  7. 7.
    Mandyam K, Loughin T, Jumpponen A. (2010) Isolation and morphological and metabolic characterization of common endophytes in annually burned tallgrass prairie. Mycologia 102:813–821 . doi:  https://doi.org/10.3852/09-212
  8. 8.
    Peterson RL, Wagg C, Pautler M (2008) Associations between microfungal endophytes and roots: do structural features indicate function? Botany 456:445–456.  https://doi.org/10.1139/B08-016 CrossRefGoogle Scholar
  9. 9.
    Usuki F, Narisawa K (2007) A mutualistic symbiosis between a dark septate endophytic fungus, Heteroconium chaetospira, and a nonmycorrhizal plant, Chinese cabbage. Mycologia 99:175–184CrossRefPubMedGoogle Scholar
  10. 10.
    Schlesinger WH (1990) Evidence from chronosequence studies for a low carbon-storage potential of soils. Nature 348:232–234CrossRefGoogle Scholar
  11. 11.
    Aguiar MR, Sala OE (1999) Patch structure, dynamics and implications for the functioning of arid ecosystems. Trends Ecol Evol 14:273–277.  https://doi.org/10.1016/S0169-5347(99)01612-2 CrossRefPubMedGoogle Scholar
  12. 12.
    Tewksbury JJ, Lloyd JD (2001) Positive interactions under nurse-plants: spatial scale, stress gradients and benefactor size. Oecologia 127:425–434.  https://doi.org/10.1007/s004420000614 CrossRefPubMedGoogle Scholar
  13. 13.
    Boulton AM, Amberman KD (2006) How ant nests increase soil biota richness and abundance: a field experiment. Biodivers Conserv 15:69–82.  https://doi.org/10.1007/s10531-004-2177-7 CrossRefGoogle Scholar
  14. 14.
    Jones CG, Lawton JH, Shachak M (1996) Organisms as ecosystem engineers BT—ecosystem management: selected readings. In: Samson FB, Knopf FL (eds) Ecosystem Management. Springer, New York, pp 130–147Google Scholar
  15. 15.
    Grant WE, French NR, Folse LJ (1980) Effects of pocket gopher mounds on plant production in shortgrass prairie ecosystems. Southwest Nat 25:215–224.  https://doi.org/10.2307/3671243 CrossRefGoogle Scholar
  16. 16.
    De Bruyn L, Conacher AJ (1990) The role of termites and ants in soil modification—a review. Soil Res 28:55–93Google Scholar
  17. 17.
    Whitford WG, Kay FR (1999) Biopedturbation by mammals in deserts: a review. J Arid Environ 41:203–230.  https://doi.org/10.1006/jare.1998.0482 CrossRefGoogle Scholar
  18. 18.
    Mun H-T, Whitford WG (1997) Changes in mass and chemistry of plant roots during long-term decomposition on a Chihuahuan Desert watershed. Biol Fertil Soils 26:16–22.  https://doi.org/10.1007/s003740050336 CrossRefGoogle Scholar
  19. 19.
    Whitford WG, DiMarco R (1995) Variability in soils and vegetation associated with harvester ant (Pogonomyrmex rugosus) nests on a Chihuahuan Desert watershed. Biol Fertil Soils 20:169–173.  https://doi.org/10.1007/BF00336554 CrossRefGoogle Scholar
  20. 20.
    Dhillion SS (1999) Environmental heterogeneity, animal disturbances, microsite characteristics, and seedling establishment in a Quercus havardii community. Restor Ecol 7:399–406.  https://doi.org/10.1046/j.1526-100X.1999.72035.x CrossRefGoogle Scholar
  21. 21.
    Chew R, Whitford W (1992) A long-term positive effect of kangaroo rats (Dipodomys spectabilis) on creosotebushes (Larrea tridentata). J Arid Environ 22:375–386Google Scholar
  22. 22.
    Stolp H (1988) Microbial ecology: organisms, habitats, activities, Cambridge. Cambridge University Press, CambridgeGoogle Scholar
  23. 23.
    Desmet P, Cowling R (1999) Patch creation by fossorial rodents: a key process in the revegetation of phytotoxic arid soils. J Arid Environ 43:35–45.  https://doi.org/10.1006/jare.1999.0535 CrossRefGoogle Scholar
  24. 24.
    Kerley GIH, Whitford WG, Kay FR (2004) Effects of pocket gophers on desert soils and vegetation. J Arid Environ 58:155–166.  https://doi.org/10.1016/j.jaridenv.2003.08.001 CrossRefGoogle Scholar
  25. 25.
    Malizia AI, Kittlein MJ, Busch C (2000) Influence of the subterranean herbivorous rodent Ctenomys talarum on vegetation and soil. Z Saugetierkd 65:172–182Google Scholar
  26. 26.
    Lara N, Sassi P, Borghi CE et al (2007) Effect of herbivory and disturbances by tuco-tucos (Ctenomys mendocinus) on a plant community in the southern Puna Desert. Arct Antarct Alp Res 39:110–116CrossRefGoogle Scholar
  27. 27.
    Zhang Y, Zhang Z, Liu J (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.  https://doi.org/10.1046/j.1365-2907.2003.00020.x CrossRefGoogle Scholar
  28. 28.
    Kuznetsova TA, Kam M, Khokhlova IS, Kostina NV, Dobrovolskaya TG, Umarov MM, Degen AA, Shenbrot GI, Krasnov BR (2013) Desert gerbils affect bacterial composition of soil. Microb Ecol 66:940–949.  https://doi.org/10.1007/s00248-013-0263-7 CrossRefPubMedGoogle Scholar
  29. 29.
    Allen MF, MacMahon JA (1988) Direct VA mycorrhizal inoculation of colonizing plants by pocket gophers (Thomomys talpoides) on Mount St. Helens. Mycologia 82:754–755CrossRefGoogle Scholar
  30. 30.
    Titus JH, Nowak RS, Smith SD (2002) Soil resource heterogeneity in the Mojave Desert. J Arid Environ 52:269–292.  https://doi.org/10.1006/jare.2002.1010 CrossRefGoogle Scholar
  31. 31.
    Fracchia S, Krapovickas L, Aranda-Rickert a, Valentinuzzi VS (2011) Dispersal of arbuscular mycorrhizal fungi and dark septate endophytes by Ctenomys cf. knighti (Rodentia) in the northern Monte Desert of Argentina. J Arid Environ 75:1016–1023.  https://doi.org/10.1016/j.jaridenv.2011.04.034 CrossRefGoogle Scholar
  32. 32.
    Abraham E, del Valle HF, Roig F, Torres L, Ares JO, Coronato F, Godagnone R (2009) Overview of the geography of the Monte Desert biome (Argentina). J Arid Environ 73:144–153.  https://doi.org/10.1016/j.jaridenv.2008.09.028 CrossRefGoogle Scholar
  33. 33.
    Aranda-Rickert A, Diez P, Marazzi B (2014) Extrafloral nectar fuels ant life in deserts. AoB Plants 6:plu068.  https://doi.org/10.1093/aobpla/plu068 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Bisigato AJ, Villagra PE, Ares JO, Rossi BE (2009) Vegetation heterogeneity in Monte Desert ecosystems: a multi-scale approach linking patterns and processes. J Arid Environ 73:182–191.  https://doi.org/10.1016/j.jaridenv.2008.09.001 CrossRefGoogle Scholar
  35. 35.
    Cook J, Lessa E (1998) Are rates of diversification in subterranean south american tuco-tucos (genus ctenomys, rodentia: octodontidae) unusually high? Evolution 52:1521–1527PubMedGoogle Scholar
  36. 36.
    Morgan CC, Verzi DH (2006) Morphological diversity of the humerus of the South American subterranean rodent Ctenomys (Rodentia, Ctenomyidae). J Mammal 87:1252–1260.  https://doi.org/10.1644/06-MAMM-A-033R1.1 CrossRefGoogle Scholar
  37. 37.
    Pearson OP (1984) Taxonomy and natural history of some fossorial rodents of Patagonia, southern Argentina. J Zool 202:225–237.  https://doi.org/10.1111/j.1469-7998.1984.tb05952.x CrossRefGoogle Scholar
  38. 38.
    Reig OA (1970) Ecological notes on the fossorial octodont rodent Spalacopus Cyanus (Molina). J Mammal 51:592–601CrossRefGoogle Scholar
  39. 39.
    Valentinuzzi VS, Oda GA, Araujo JF, Ralph MR (2009) Circadian pattern of wheel-running activity of a South American subterranean rodent (Ctenomys cf knightii). Chronobiol Int 26:14–27.  https://doi.org/10.1080/07420520802686331 CrossRefPubMedGoogle Scholar
  40. 40.
    Tachinardi P, Bicudo JEW, Oda GA, Valentinuzzi VS (2014) Rhythmic 24 h variation of core body temperature and locomotor activity in a subterranean rodent (Ctenomys aff. knighti)—the tuco-tuco. PLoS One 9:1–8.  https://doi.org/10.1371/journal.pone.0085674 CrossRefGoogle Scholar
  41. 41.
    Mares MA, Hulse AC (1977) Patterns of some vertebrate communities in creosote bush deserts. Creosote Bush Biol Chem Larrea New World Deserts, Dowden, Hutchinson Ross, Stroudsburg, Pennsylvania 209–226Google Scholar
  42. 42.
    Borruel N, Campos CM, Giannoni SM, Borghi CE (1998) Effect of herbivorous rodents (cavies and tuco-tucos) on a shrub community in the Monte Desert, Argentina. J Arid Environ 39:33–37CrossRefGoogle Scholar
  43. 43.
    Altuna CA, Francescoli G, Tassino B (1999) Ecoetología y conservación de mamíferos subterráneos de distribución restringida: el caso de Ctenomys pearsoni. Etologia 7:47–54Google Scholar
  44. 44.
    Sieverding E, Friedrichsen J, Suden W (1991) Vesicular-arbuscular mycorrhiza management in tropical agrosystems. Dtsch Gesellschaft fuer Tech ZusammenarbeitGoogle Scholar
  45. 45.
    Barrow JR (2003) Atypical morphology of dark septate fungal root endophytes of Bouteloua in arid southwestern USA rangelands. Mycorrhiza 13:239–247.  https://doi.org/10.1007/s00572-003-0222-0 CrossRefPubMedGoogle Scholar
  46. 46.
    McGonigle TP, Miller MH, Evans DG et al (1990) A new method which gives an objective measure of colonization of roots by vesicular arbuscular mycorrhizal fungi. New Phytol 115:495–501.  https://doi.org/10.1111/j.1469-8137.1990.tb00476.x CrossRefGoogle Scholar
  47. 47.
    Fisher RA, Yates F (1963) Statistical tables for biological, agricultural and medical research, edited by RA Fisher and F. Yates. Oliver and Boyd, EdinburghGoogle Scholar
  48. 48.
    An ZQ, Hendrix JW, Hershman DE, Henson GT (1990) Evaluation of the “most probable number”(MPN) and wet-sieving methods for determining soil-borne populations of endogonaceous mycorrhizal fungi. Mycol 82:576–581CrossRefGoogle Scholar
  49. 49.
    Anderson J (1982) Soil respiration. In: Methods of soil analysis. Soil Science Society of America, Madison, Wisconsin, USA, pp 831–871Google Scholar
  50. 50.
    Sparks DL, Page AL, Helmke PA, et al (1996) Methods of soil analysis: chemical methods. In: Chemical methods, 3rd ed. American Society of Agronomy, Madison: ASA and SSSA, p 1390Google Scholar
  51. 51.
    Bray RH, Kurtz LT (1945) Determination of total, organic, and available forms of soil phosphorus in soil. Soil Sci 59:39–46CrossRefGoogle Scholar
  52. 52.
    Daniel PE, Marbán LG (1989) Adaptación de un método espectrofotométrico reductivo para la determinación de nitratos en estractos de suelos. Boletín la Asoc Argentina la Cienc del Suelo 583:3–8Google Scholar
  53. 53.
    Colman EA (1946) A laboratory procedure for determining the field capacity of soils. Soil Sci 67:277–283Google Scholar
  54. 54.
    R Core Team (2017) R: A language and environment for statistical computingGoogle Scholar
  55. 55.
    Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Rose SL, Youngberg CT (1981) Tripartite associations in snowbrush (Ceanothus velutinus): effect of vesicular–arbuscular mycorrhizae on growth, nodulation, and nitrogen fixation. Can J Bot 59:34–39CrossRefGoogle Scholar
  57. 57.
    Trappe JM (1981) Mycorrhizae and productivity of arid and semiarid rangelands. In: Advances in food-producing systems for arid and semiarid lands, Part A. Elsevier, pp 581–599Google Scholar
  58. 58.
    Mejstřík VK, Cudlin P (1983) Mycorrhiza in some plant desert species in Algeria. In: Tree root systems and their mycorrhizas. Springer, pp 363–366Google Scholar
  59. 59.
    Bloss HE, Walker C (1987) Some endogonaceous mycorrhizal fungi of the Santa Catalina mountains in Arizona. Mycologia 79:649–654CrossRefGoogle Scholar
  60. 60.
    Carrillo-Garcia A, León De La Luz JL, Bashan Y, Bethlenfalvay GJ (1999) Nurse plants, mycorrhizae, and plant establishment in a disturbed area of the Sonoran Desert. Restor Ecol 7:321–335.  https://doi.org/10.1046/j.1526-100X.1999.72027.x CrossRefGoogle Scholar
  61. 61.
    Bethlenfalvay GJ, Dakessian S, Pacovsky RS (1984) Mycorrhizae in a southern California desert: ecological implications. Can J Bot 62:519–524.  https://doi.org/10.1139/b84-077 CrossRefGoogle Scholar
  62. 62.
    Cui M, Nobel PS (1992) Nutrient status, water uptake and gas exchange for three desert succulents infected with mycorrhizal fungi. New Phytol 122:643–649.  https://doi.org/10.1111/j.1469-8137.1992.tb00092.x CrossRefGoogle Scholar
  63. 63.
    Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance generated by plant/fungal symbiosis. Science 298:1581.  https://doi.org/10.1126/science.1072191 CrossRefPubMedGoogle Scholar
  64. 64.
    Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793.  https://doi.org/10.1111/j.1469-8137.2010.03611.x CrossRefPubMedGoogle Scholar
  65. 65.
    Rodriguez RJ, Redman RS, Henson JM (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strateg Glob Chang 9:261–272.  https://doi.org/10.1023/B:MITI.0000029922.31110.97 CrossRefGoogle Scholar
  66. 66.
    Knapp DG, Kovács GM, Zajta E, Groenewald JZ, Crous PW (2015) Dark septate endophytic pleosporalean genera from semiarid areas. Persoonia 35:87–100.  https://doi.org/10.3767/003158515X687669 CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    McGee PA (1989) Variation in propagule numbers of vesicular-arbuscular mycorrhizal fungi in a semi-arid soil. Mycol Res 92:28–33CrossRefGoogle Scholar
  68. 68.
    N R, P J, Barea J (1996) Assessment of natural mycorrhizal potential in a desertified semiarid ecosystem. Appl Environ Microbiol 62:842–847Google Scholar
  69. 69.
    Sigüenza C, Espejel I, Allen EB (1996) Seasonality of mycorrhizae in coastal sand dunes of Baja California. Mycorrhiza 6:151–157CrossRefGoogle Scholar
  70. 70.
    He X, Mouratov S, Steinberger Y (2002) Temporal and spatial dynamics of vesicular-arbuscular mycorrhizal fungi under the canopy of Zygophyllum dumosum Boiss. in the Negev Desert. J Arid Environ 52:379–387.  https://doi.org/10.1006/jare.2002.1000 CrossRefGoogle Scholar
  71. 71.
    Ayarbe JP, Kieft TL (2000) Mammal mounds stimulate microbial activity in a semiarid shrubland. Ecology 81:1150–1154CrossRefGoogle Scholar
  72. 72.
    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 33:92–98CrossRefGoogle Scholar
  73. 73.
    Nadler A, Steinberger Y (1993) Trends in structure, plant growth, and microorganism interrelations in the soil. Soil Sci 155:114–122CrossRefGoogle Scholar
  74. 74.
    Wetzel PR, Van Der Valk AG, Newman S et al (2009) Heterogeneity of phosphorus distribution in a patterned landscape, the Florida Everglades. Plant Ecol 200:83–90.  https://doi.org/10.1007/s11258-008-9449-3 CrossRefGoogle Scholar
  75. 75.
    Schlesinger WH, Bernhardt E Biogeochemistry: an analasis of global changeGoogle Scholar
  76. 76.
    Holford ICR, Mattingly GEG (1976) Phosphate adsorption and availability plant of phosphate. Plant Soil 44:377–389CrossRefGoogle Scholar
  77. 77.
    Cameron SL (1998) Colonization of Populus tremuloides seedlings by the fungus Phialocephala fortinii in the presence of the ectomycorrhal fungus Thelephora terrestris. The University of Guelph, GuelphGoogle Scholar
  78. 78.
    Johnson DL (1990) Biomantle evolution and the redistribution of earth materials and artifacts. Soil Sci 149:84–102CrossRefGoogle Scholar
  79. 79.
    Camargo-Ricalde SL, Dhillion SS (2003) Endemic Mimosa species can serve as mycorrhizal “resource islands” within semiarid communities of the Tehuacán-Cuicatlán Valley, Mexico. Mycorrhiza 13:129–136.  https://doi.org/10.1007/s00572-002-0206-5 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Victoria Miranda
    • 1
  • Carolina Rothen
    • 1
  • Natalia Yela
    • 1
  • Adriana Aranda-Rickert
    • 1
  • Johana Barros
    • 1
  • Javier Calcagno
    • 2
  • Sebastián Fracchia
    • 1
  1. 1.Centro Regional de Investigaciones Científicas y Transferencia Tecnológica de La Rioja (CRILAR-CONICETProvincia de La Rioja, UNLAR, SEGEMAR, UNCa)Anillaco La RiojaArgentina
  2. 2.Centro de Estudios Biomédicos, Biotecnológicos, Ambientales y de Diagnóstico (CEBBAD), Departamento de Ciencias Naturales y AntropológicasCONICETBuenos AiresArgentina

Personalised recommendations