Skip to main content
Log in

Consumption of grass endophytes alters the ultraviolet spectrum of vole urine

  • Plant-Animal Interactions - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Fungal endophytes of grasses are known to benefit their hosts directly by increasing resistance to herbivores through mycotoxins. We propose and test assumptions of a novel hypothesis according to which fungal endophytes of grasses may benefit their hosts also indirectly by increasing the conspicuousness of a mammalian herbivore, the field vole (Microtus agrestis), to its avian predators by enhancing the ultraviolet visibility of vole urine. We found that field voles feeding on endophyte-infected meadow ryegrass (Lolium pratense) lost body mass, while voles feeding on non-infected meadow ryegrass gained mass. More interestingly, the maximum peak intensity of ultraviolet fluorescence in the urine of voles feeding on endophyte-infected grass shifted from over 380 nm to circa 370 nm, which is the suggested maximum sensitivity of the ultraviolet pigments in the eyes of vole-eating raptors. Therefore, grazing on endophyte-infected grass alters the ultraviolet spectrum of vole urine, thus potentially enhancing its visibility to avian predators.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2a, b
Fig. 3

Similar content being viewed by others

References

  • Aldrich CG, Rhodes MT, Miner JL, Kerley MS, Paterson JA (1993) The effects of endophyte-infected tall fescue consumption and use of a dopamine antagonist on intake, digestibility, body-temperature, and blood-constituents in sheep. J Anim Sci 71:158–163

    PubMed  CAS  Google Scholar 

  • Andersson S, Prager M (2006) Quantifying colors. In: Hill GE, McGraw KJ (eds) Bird coloration. Volume 1. Mechanisms and measurements. Harvard University Press, Cambridge, pp 41–89

    Google Scholar 

  • Barger JL, Tannenbaum MG (1998) Consumption of endophyte-infected fescue seeds and osmoregulation in white-footed mice. J Mammal 79:464–474

    Article  Google Scholar 

  • Batzli GO (1986) Nutritional ecology of the California vole––effects of food quality on reproduction. Ecology 67:406–412

    Article  Google Scholar 

  • Bennett ATD, Cuthill IC (1994) Ultraviolet vision in birds: what is its function? Vision Res 34:1471–1478

    Article  PubMed  CAS  Google Scholar 

  • Bultman TL, Ganey DT (1995) Induced resistance to fall armyworm (Lepidoptera: Noctuidae) mediated by a fungal endophyte. Environ Entomol 24:1196–1200

    Google Scholar 

  • Bultman TL, Bell G, Martin WD (2004) A fungal endophyte mediates reversal of wound-induced resistance and constrains tolerance in a grass. Ecology 85:679–685

    Article  Google Scholar 

  • Chávez AE, Bozinovic F, Peichl L, Palacios AG (2003) Retinal spectral sensitivity, fur coloration, and urine reflectance in the genus Octodon (Rodentia): implications for visual ecology. Invest Ophthalmol Vis Sci 44:2290–2296

    Article  PubMed  Google Scholar 

  • Cheplick GP, Clay K (1988) Acquired chemical defenses in grasses––the role of fungal endophytes. Oikos 52:309–318

    Article  Google Scholar 

  • Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69:10–16

    Article  Google Scholar 

  • Clay K (2001) Symbiosis and the regulation of communities. Am Zool 41:810–824

    Article  Google Scholar 

  • Cole RF, Batzli GO (1979) Nutrition and population dynamics of the prairie vole, Microtus ochrogaster, in Central Illinois. J Anim Ecol 48:455–470

    Article  Google Scholar 

  • Coley AB, Fribourg HA, Pelton MR, Gwinn KD (1995) Effects of tall fescue endophyte infestation on relative abundance of small mammals. J Environ Qual 24:472–475

    Article  CAS  Google Scholar 

  • Conover MR (1998) Impact of consuming tall fescue leaves with the endophytic fungus, Acremonium coenophialum, on meadow voles. J Mammal 79:457–463

    Article  Google Scholar 

  • Conover MR (2003) Impact of the consumption of endophyte-infected perennial ryegrass by meadow voles. Agric Ecosyst Environ 97:199–203

    Article  Google Scholar 

  • Cuthill IC, Partridge JC, Bennett ATD, Church SC, Hart NS, Hunt S (2000) Ultraviolet vision in birds. Adv Study Behav 29:159–214

    Article  Google Scholar 

  • De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • de Sassi C, Müller CB, Krauss J (2006) Fungal plant endosymbionts alter life history and reproductive success of aphid predators. Proc R Soc B 273:1301–1306

    Article  PubMed  Google Scholar 

  • Desjardins C, Maruniak JA, Bronson FH (1973) Social rank in house mice: differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182:939–941

    Article  PubMed  CAS  Google Scholar 

  • Durham WF, Tannenbaum MG (1998) Effects of endophyte consumption on food intake, growth, and reproduction in prairie voles. Can J Zool 76:960–969

    Article  CAS  Google Scholar 

  • Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63:1–27

    Article  Google Scholar 

  • Fortier GM, Bard N, Jansen M, Clay K (2000) Effects of tall fescue endophyte infection and population density on growth and reproduction in prairie voles. J Wildl Manage 64:122–128

    Article  Google Scholar 

  • Goldsmith TH (1990) Optimization, constraint, and history in the evolution of eyes. Q Rev Biol 65:281–322

    Article  PubMed  CAS  Google Scholar 

  • Halle S (1993) Diel pattern of predation risk in microtine rodents. Oikos 68:510–518

    Article  Google Scholar 

  • Huitu O, Jokinen I, Korpimäki E, Koskela E, Mappes T (2007) Phase dependence in winter physiological condition of cyclic voles. Oikos 116:565–577

    Article  CAS  Google Scholar 

  • Hämet-Ahti L, Suominen J, Ulvinen T, Uotila P (eds) (1998) Retkeilykasvio (Field flora of Finland), 4th edn. Finnish Museum of Natural History, Botanical Museum, Helsinki

  • Jönsson KI (1997) Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78:57–66

    Article  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University Chicago Press, Chicago

    Google Scholar 

  • Kellie A, Dain SJ, Banks PB (2004) Ultraviolet properties of Australian mammal urine. J Comp Physiol A 190:429–435

    Article  CAS  Google Scholar 

  • Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144

    Article  PubMed  CAS  Google Scholar 

  • Koivula M, Viitala J (1999) Rough-legged buzzards use vole scent marks to assess hunting areas. J Avian Biol 30:329–332

    Article  Google Scholar 

  • Koivula M, Korpimäki E, Viitala J (1997) Do Tengmalm’s owls see vole scent marks visible in ultraviolet light? Anim Behav 54:873–877

    Article  PubMed  Google Scholar 

  • Koivula M, Koskela E, Viitala J (1999) Sex and age-specific differences in ultraviolet reflectance of scent marks of bank voles (Clethrionomys glareolus). J Comp Physiol A 185:561–564

    Article  PubMed  CAS  Google Scholar 

  • Lakowicz JR (1999) Principles of fluorescence spectroscopy, 2nd edn. Kluwer, Plenum, New York

    Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary

    Google Scholar 

  • Montgomerie R (2006) Analyzing colors. In: Hill GE, McGraw KJ (eds) Bird coloration. Volume 1. Mechanisms and measurements. Harvard University Press, Cambridge, pp 90–147

    Google Scholar 

  • Myllymäki A (1977) Interactions between the field vole Microtus agrestis and its microtine competitors in Central-Scandinavian populations. Oikos 29:570–580

    Article  Google Scholar 

  • Mäntylä E, Klemola T, Haukioja E (2004) Attraction of willow warblers to sawfly-damaged mountain birches: novel function of inducible plant defences? Ecol Lett 7:915–918

    Article  Google Scholar 

  • Nishida R (2002) Sequestration of defensive substances from plants by Lepidoptera. Annu Rev Entomol 47:57–92

    Article  PubMed  CAS  Google Scholar 

  • Omacini M, Chaneton EJ, Ghersa CM, Müller CB (2001) Symbiotic fungal endophytes control insect host-parasite interaction webs. Nature 409:78–81

    Article  PubMed  CAS  Google Scholar 

  • Saha DC, Jackson MA, Johnson-Cicalese JM (1988) A rapid staining method for detection of endophyte fungi in turf and forage grasses. Phytopathology 78:237–239

    Article  CAS  Google Scholar 

  • Saikkonen K, Faeth SH, Helander M, Sullivan TJ (1998) Fungal endophytes: a continuum of interactions with host plants. Annu Rev Ecol Syst 29:319–343

    Article  Google Scholar 

  • Saikkonen K, Ahlholm J, Helander M, Lehtimäki S, Niemeläinen O (2000) Endophytic fungi in wild and cultivated grasses in Finland. Ecography 23:360–366

    Article  Google Scholar 

  • Saikkonen K, Lehtonen P, Helander M, Koricheva J, Faeth S (2006) Model systems in ecology: dissecting the grass-endophyte literature. Trends Plant Sci 11:428–433

    Article  PubMed  CAS  Google Scholar 

  • Siegel MR, Bush LP (1997) Toxin production in grass/endophyte associations. In: Carroll GC, Tudzynski P (eds) The Mycota v. plant relationships, part B. Springer, Berlin, pp 185–208

    Google Scholar 

  • Sullivan TJ, Rodstrom J, Vandop J, Librizzi J, Graham C, Schardl CL, Bultman TL (2007) Symbiont-mediated changes in Lolium arundinaceum inducible defenses: evidence from changes in gene expression and leaf composition. New Phytol 176:673–679

    Article  PubMed  CAS  Google Scholar 

  • Takabayashi J, Dicke M (1996) Plant-carnivore mutualism through herbivore-induced carnivore attractants. Trends Plant Sci 1:109–113

    Article  Google Scholar 

  • Varney DR, Ndefru M, Jones SL, Newsome R, Siegel MR, Zavos PM (1987) The effect of feeding endophyte infected tall fescue seed on reproductive-performance in female rats. Comp Physiol Biochem C 87:171–175

    Article  CAS  Google Scholar 

  • Viitala J, Korpimäki E, Palokangas P, Koivula M (1995) Attraction of kestrels to vole scent marks visible in ultraviolet light. Nature 373:425–427

    Article  CAS  Google Scholar 

  • Vorobyev M, Osorio D, Bennett ATD, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621–633

    Article  PubMed  CAS  Google Scholar 

  • Zavos PM, Salim B, Jackson JA, Varney DR, Siegel MR, Hemken RW (1986) Effect of feeding tall fescue seed infected by endophytic fungus (Acremonium coenophialum) on reproductive performance in male rats. Theriogenology 25:281–290

    Article  PubMed  CAS  Google Scholar 

  • Zynel CA, Wunder BA (2002) Limits to food intake by the Prairie Vole: effects of time for digestion. Funct Ecol 16:58–66

    Article  Google Scholar 

Download references

Acknowledgments

We thank Peter Banks and anonymous referees for helpful comments on the manuscript, Marjo Anttila for help in rearing the plants, Sini Isola for helping with the voles and Riitta Koivikko for analyzing fluorescence from the urine samples. This work was supported by grants from the Academy of Finland (no. 106036 to O. H., no. 202799 to K. S.). This research adhered to the Association for the Study of Animal Behaviour/Animal Behavior Society Guidelines for the Use of Animals in Research, the legal requirements of Finland and all institutional guidelines.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Otso Huitu.

Additional information

Communicated by Anssi Laurila.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huitu, O., Helander, M., Lehtonen, P. et al. Consumption of grass endophytes alters the ultraviolet spectrum of vole urine. Oecologia 156, 333–340 (2008). https://doi.org/10.1007/s00442-008-0984-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-008-0984-3

Keywords

Navigation