Evolutionary Ecology

, Volume 27, Issue 6, pp 1069–1080

Friend or foe? Disparate plant–animal interactions of two congeneric rodents

  • Michal Samuni-Blank
  • Zeev Arad
  • M. Denise Dearing
  • Yoram Gerchman
  • William H. Karasov
  • Ido Izhaki
Original Paper

Abstract

Food and water resources are limiting factors for animals in desert ecosystems. Fleshy fruits are a rare water source in deserts and when available they tend to attract a wide variety of organisms. Here we show that two congeneric rodent species, Acomys cahirinus and A. russatus, employ different fruit eating strategies that result in either dispersal or predation of the small seeds of the desert plant Ochradenus baccatus. The nocturnal A. cahirinus leaves intact seeds when consuming O. baccatus fruits and thus, acts mainly as a seed disperser; whereas the diurnal A. russatus consumes the whole fruit and digests the seeds and thus, acts mainly as a seed predator. Acomysrussatus is subjected to the toxic products of the glucosinolates-myrosinase system found in O. baccatus fruits. Acomyscahirinus avoids the toxic compounds by consuming the pulp only, which contains glucosinolates but not the seeds that contain the enzyme that activates them. We suggest that the behavioral responses exhibited by A. russatus are the result of physiological adaptations to whole fruit consumption that are absent in A. cahirinus. Our results shed new light on the ecological divergence of the two congeneric species.

Keywords

Desert Fruits Glucosinolates Rodents Secondary compounds Seed dispersal 

References

  1. Abramsky Z (1983) Experiments on seed predation by rodents and ants in the Israeli desert. Oecologia 57:328–332CrossRefGoogle Scholar
  2. Beck MJ, Vander Wall SB (2010) Seed dispersal by scatter-hoarding rodents in arid environments. Ecology 98:1300–1309CrossRefGoogle Scholar
  3. Ben-Moshe A, Dayan T, Simberloff D (2001) Convergence in morphological patterns and community organization between Old and New World rodent guilds. Am Nat 158:484–495PubMedCrossRefGoogle Scholar
  4. Blendinger PG, Díaz-Vélez MC (2010) Experimental Weld test of spatial variation in rodent predation of nuts relative to distance and seed density. Oecologia 163:415–423PubMedCrossRefGoogle Scholar
  5. Briani DC, Guimaraes PR (2007) Seed predation and fruit damage of Solanum lycocarpum (Solanaceae) by rodents in the cerrado of central Brazil. Acta Oecol 31:8–12CrossRefGoogle Scholar
  6. Bronstein JL, Izhaki I, Nathan R, Tewksbury JJ, Spiegel O, Lotan A, Altstein O, Dennis AJ, Schupp EW, Green RJ (2007) Fleshy-fruited plants and frugivores in desert ecosystems In: Dennis AJ, Schupp EW, Green RJ, Westcott DW (eds). Seed dispersal: theory and its application in a changing world. Cab International, Wallingford, pp 148–177Google Scholar
  7. Brown JH, Davidson DW (1977) Competition between seed-eating rodents and ants in desert ecosystems. Science 196:880–882PubMedCrossRefGoogle Scholar
  8. Brown JH, Heske EJ (1990) Control of a desert-grassland transition by a keystone rodent guild. Science 250:1705–1707PubMedCrossRefGoogle Scholar
  9. Brown JH, Davidson DW, Reichman OJ (1979a) An experimental study of competition between seed-eating desert rodents and ants. Am Zool 19:1129–1143Google Scholar
  10. Brown JH, Reichman OJ, Davidson DW (1979b) Granivory in desert ecosystems. Annu Rev Ecol Syst 10:201–227CrossRefGoogle Scholar
  11. Cipollini ML, Levey DJ (1997a) Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am Nat 150:346–372PubMedCrossRefGoogle Scholar
  12. Cipollini ML, Levey DJ (1997b) Why are some fruits toxic? Glycoalkaloids in Solanum and fruit choice by vertebrates. Ecology 78:782–798Google Scholar
  13. Davidson DW, Brown JH, Inouye RS (1980) Competition and the structure of granivore communities. Bioscience 30:233–238CrossRefGoogle Scholar
  14. Davidson DW, Inouye RS, Brown JH (1984) Granivory in a desert ecosystem: experimental evidence for indirect facilitation of ants by rodents. Ecology 65:1780–1786CrossRefGoogle Scholar
  15. Dearing MD, Foley WJ, McLean S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annu Rev Ecol Evol Syst 36:169–189CrossRefGoogle Scholar
  16. Ehrhardt N, Heldmaier G, Exner C (2005) Adaptive mechanisms during food restriction in Acomys russatus: the use of torpor for desert survival. J Comp Physiol B 175:193–200PubMedCrossRefGoogle Scholar
  17. Forget PM, Milleron T (1991) Evidence for secondary seed dispersal by rodents in Panama. Oecologia 87:596–599CrossRefGoogle Scholar
  18. Gautier-Hion A, Duplantier JM, Quris R, Feer F, Sourd C, Decoux JP, Dubost G, Emmons L, Erard C, Hecketsweiler P (1985) Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65:324–337CrossRefGoogle Scholar
  19. Gutman R, Choshniak I, Kronfeld-Schor N (2006) Defending body mass during food restriction in Acomys russatus: a desert rodent that does not store food. Am J Physiol 290:881–891Google Scholar
  20. Haim A, Borut A (1981) Heat production and dissipation in golden spiny mice, Acomys russatus, from two extreme habitats. J Comp Physiol 142:445–450Google Scholar
  21. Haim A, Yedidia I, Haim D, Zisapel N (1994) Photoperiodicity in daily rhythms of body temperature, food and energy intake of the golden spiny mouse (Acomys russatus). Isr J Zool 40:145–150Google Scholar
  22. Haim A, Alma A, Neuman A (2005) Body mass is a thermoregulatory adaptation of diurnal rodents to the desert environment. J Therm Biol 31:168–171CrossRefGoogle Scholar
  23. Herrera CM (1982) Defense of ripe fruit from pests: its significance in relation to plant-disperser interactions. Am Nat 120:218–241CrossRefGoogle Scholar
  24. Heske EJ, Brown JH, Mistry S (1994) Long-term experimental study of a Chihuahuan Desert rodent community: 13 years of competition. Ecology 75:438–445CrossRefGoogle Scholar
  25. Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228CrossRefGoogle Scholar
  26. Izhaki I (2002) Emodin—a secondary metabolite with multiple ecological functions in higher plants (a review). New Phytol 155:205–217CrossRefGoogle Scholar
  27. Jansen PA, Bongers F, Hemerik L (2004) Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent. Ecol Monogr 74:569–589CrossRefGoogle Scholar
  28. Jones M, Dayan T (2000) Foraging behavior and microhabitat use by spiny mice, Acomys cahirinus and A. russatus, in the presence of Blanford’s fox (Vulpes cana) odor. J Chem Ecol 26:455–469CrossRefGoogle Scholar
  29. Kam M, Degen A (1991) Diet selection and energy and water budgets of the common spiny mouse Acomys cahirinus. J Zool 225:285–292CrossRefGoogle Scholar
  30. Kam M, Degen AA (1993) Effect of dietary preformed water on energy and water budgets of two sympatric desert rodents, Acomys russatus and Acomys cahirinus. J Zool 231:51–59CrossRefGoogle Scholar
  31. Kelt DA, Meserve PL, Gutiérrez JR (2004) Seed removal by small mammals, birds and ants in semi-arid Chile, and comparison with other systems. J Biogeogr 31:931–942CrossRefGoogle Scholar
  32. Kronfeld N, Dayan T, Zisapel N, Haim A (1994) Coexisting population of Acomys cahirinus and A. russatus: a preliminary report. Isr J Zool 40:177–183Google Scholar
  33. Kronfeld-Schor N, Dayan T (1999) The dietary basis for temporal partitioning: food habits of coexisting Acomys species. Oecologia 121:123–128CrossRefGoogle Scholar
  34. Leaver L, Daly M (1998) Effects of food preference on scatter-hoarding by kangaroo rats (Dipodomys merriami). Behaviour 135:823–832CrossRefGoogle Scholar
  35. Levy O, Dayan T, Kronfeld-Schor N (2011) Interspecific competition and torpor in golden spiny mice: two sides of the energy-acquisition coin. Integr Comp Biol 51:441–448PubMedCrossRefGoogle Scholar
  36. Longland WS, Jenkins SH, Vander Wall SB, Veech JA, Pyare SS (2001) Seedling recruitment in Oryzopsis hymenoides: are desert granivores mutualists or predators? Ecology 82:3131–3148Google Scholar
  37. Lotan A, Izhaki I (2013) Could abiotic environment shape fleshy fruit traits? A field study of the desert shrub Ochradenus baccatus. J Arid Environ 92:34–41Google Scholar
  38. Maron JL, Simms EL (1997) Effect of seed predation on seed bank size and seedling recruitment of bush lupine (Lupinus arboreus). Oecologia 111:76–83CrossRefGoogle Scholar
  39. Matile PH (1980) The mustard oil bomb. Compartmentation of the myrosinase system. Biochem Physiol Pflanz 175:722–731CrossRefGoogle Scholar
  40. Moles AT, Warton DI, Westoby M (2003) Do small-seeded species have higher survival through seed predation than large-seeded species? Ecology 84:3148–3161CrossRefGoogle Scholar
  41. Norconk MA, Grafton BW, Conklin-Brittain NL (1998) Seed dispersal by neotropical seed predators. Am J Primatol 45:103–126PubMedCrossRefGoogle Scholar
  42. Noy-Meir I (1973) Desert ecosystems: environment and producers. Annu Rev Ecol Syst 4:25–51CrossRefGoogle Scholar
  43. Price MV, Joyner JW (1997) What resources are available to desert granivores: seed rain or soil seed bank? Ecology 78:764–773Google Scholar
  44. Rodgerson L (1998) Mechanical defense in seeds adapted for ant dispersal. Ecology 79:1669–1677CrossRefGoogle Scholar
  45. Ronel M, Lev-Yadun S (2012) The spiny, thorny and prickly plants in the flora of Israel. Bot J Linn Soc 168:344–352CrossRefGoogle Scholar
  46. Samuni-Blank M, Izhaki I, Dearing MD, Gerchman Y, Trabelcy B, Lotan A, Karasov WH, Arad Z (2012) Intraspecific directed deterrence by the mustard oil bomb in a desert plant. Curr Biol 22:1218–1220PubMedCrossRefGoogle Scholar
  47. Seifert AW, Kiama SG, Seifert MG, Goheen JR, Palmer TM, Maden M (2012) Skin shedding and tissue regeneration in African spiny mice (Acomys). Nature 489:561–565PubMedCrossRefGoogle Scholar
  48. Shkolnik A (1966) Studies in the comparative biology of Israel’s two species of spiny mice (genus Acomys). Department of Zoology, Hebrew University, Jerusalem, Israel, PhD dissertationGoogle Scholar
  49. Shkolnik A, Borut A (1969) Temperature and water relations in two species of spiny mice (Acomys). Am Soc Mamm 50:245–255Google Scholar
  50. Sork VL (1983) Mammalian seed dispersal of pignut hickory during three fruiting seasons. Ecology 64:1049–1056CrossRefGoogle Scholar
  51. Taraborelli P, Borruel N, Mangeaud A (2009) Ability of murid rodents to find buried seeds in the Monte Desert. Ethology 115:201–209CrossRefGoogle Scholar
  52. Tewksbury JJ, Nebhan GP (2001) Seed dispersal. Directed deterrence by capsaicin in chilies. Nature 41:403–404CrossRefGoogle Scholar
  53. Torregrossa AM, Dearing MD (2009) Nutritional toxicology of mammals: regulated intake of plant secondary compounds. Funct Ecol 23:48–56CrossRefGoogle Scholar
  54. Vander Wall SB (1990) Food hoarding in animals. University of Chicago Press, ChicagoGoogle Scholar
  55. Vander Wall SB (1993) Salivary water loss to seeds in yellow pine chipmunks and Merriam’s kangaroo rats. Ecology 74:1307–1312CrossRefGoogle Scholar
  56. Vander Wall SB (2010) How plants manipulate the scatter-hoarding behaviour of seed-dispersing animals. Phil Tran Roy Soc B 365:989–997CrossRefGoogle Scholar
  57. Vander Wall SB, Kuhn KM, Gworek JR (2005) Two-phase seed dispersal: linking the effects of frugivorous birds and seed-caching rodents. Oecologia 145:281–286CrossRefGoogle Scholar
  58. Velho N, Isvaran K, Datta A (2012) Rodent seed predation: effects on seed survival, recruitment, abundance, and dispersion of bird-dispersed tropical trees. Oecologia 169:995–1004PubMedCrossRefGoogle Scholar
  59. Volobouev V, Auffray JC, Debat V, Denys C, Gautun JC, Tranier M (2007) Species delimitation in the Acomys cahirinusdimidiatus complex (Rodentia, Muridae) inferred from chromosomal and morphological analyses. Biol J Linnean Soc 91:203–214CrossRefGoogle Scholar
  60. Vonshak M, Dayan T, Kronfeld-Schor N (2009) Arthropods as a prey resource: patterns of diel, seasonal, and spatial availability. J Arid Environ 73:458–462CrossRefGoogle Scholar
  61. Wang B, Chen J (2009) Seed size, more than nutrient or tannin content, affects seed caching behavior of a common genus of Old World rodents. Ecology 90:3023–3032PubMedCrossRefGoogle Scholar
  62. Wittstock U, Haliker BA (2002) Glucosinolate research in the Arabidopsis era. Trends Plant Sci 7:263–270PubMedCrossRefGoogle Scholar
  63. Wolfe LM, Burns JL (2001) A rare continual flowering strategy and its influence on offspring quality in a gynodioecious plant. Am J Bot 88:1419–1423PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Michal Samuni-Blank
    • 1
  • Zeev Arad
    • 1
  • M. Denise Dearing
    • 2
  • Yoram Gerchman
    • 3
  • William H. Karasov
    • 4
  • Ido Izhaki
    • 5
  1. 1.Department of BiologyTechnion-Israel Institute of TechnologyHaifaIsrael
  2. 2.Department of BiologyUtah UniversitySalt Lake CityUSA
  3. 3.Biology and EnvironmentHaifa University in OranimTivonIsrael
  4. 4.Department of Forest and Wildlife EcologyUniversity of WisconsinMadisonUSA
  5. 5.Department of Evolutionary and Environmental BiologyUniversity of HaifaHaifaIsrael

Personalised recommendations