Signaling from below: rodents select for deeper fruiting truffles with stronger volatile emissions

Stephens, Ryan B.; Trowbridge, Amy M.; Ouimette, Andrew P.; Knighton, W. Berk; Hobbie, Erik A.; Stoy, Paul C.; Rowe, Rebecca J.

doi:10.1002/ecy.2964

Title: Signaling from below: rodents select for deeper fruiting truffles with stronger volatile emissions

Journal Article · 23 December 2019 · Ecology

DOI: https://doi.org/10.1002/ecy.2964 · OSTI ID:1802191

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Univ. of New Hampshire, Durham, NH (United States); OSTI
Univ. of Wisconsin, Madison, WI (United States)
Univ. of New Hampshire, Durham, NH (United States)
Montana State Univ., Bozeman, MT (United States)

Many plant and fungal species use volatile organic compounds (VOCs) as chemical signals to convey information about the location or quality of their fruits or fruiting bodies to animal dispersers. Identifying the environmental factors and biotic interactions that shape fruit selection by animals is key to understanding the evolutionary processes that underpin chemical signaling. Using four Elaphomyces truffle species, we explored the role of fruiting depth, VOC emissions, and protein content in selection by five rodent species. We used stable isotope analysis of nitrogen (δ15N) in truffles to estimate fruiting depth, proton-transfer-reaction mass spectrometry to determine volatile emission composition, and nitrogen concentrations to calculate digestible protein of truffles. We coupled field surveys of truffle availability with truffle spore loads in rodent scat to determine selection by rodents. Despite presumably easier access to the shallow fruiting species, E. americanus (0.5-cm depth) and E. verruculosus (2.5-cm depth), most rodents selected for truffles fruiting deeper in the soil, E. macrosporus (4.1-cm depth) and E. bartlettii (5.0-cm depth). The deeper fruiting species had distinct VOC profiles and produced significantly higher quantities of odiferous compounds. Myodes gapperi (southern red-backed vole), a fungal specialist, also selected for truffles with high levels of digestible protein, E. verruculosus and E. macrosporus. Our results highlight the importance of chemical signals in truffle selection by rodents and suggest that VOCs are under strong selective pressures relative to protein rewards. Strong chemical signals likely allow detection of truffles deep within the soil and reduce foraging effort by rodents. Finally, for rodents that depend on fungi as a major food source, protein content may also be important in selecting truffles.

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Research Organization:: HyPerspectives Inc., Bozeman, MT (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: SC0010845

OSTI ID:: 1802191

Journal Information:: Ecology, Journal Name: Ecology Journal Issue: 3 Vol. 101; ISSN 0012-9658

Publisher:: Ecological Society of America (ESA)Copyright Statement

Country of Publication:: United States

Language:: English

References (66)

Odour thresholds of some organic compounds associated with food flavours Guadagni, D. G.; Buttery, Ron G.; Okano, S. Journal of the Science of Food and Agriculture, Vol. 14, Issue 10 https://doi.org/10.1002/jsfa.2740141014	journal	October 1963
Measurements of volatile organic compounds in the earth's atmosphere using proton-transfer-reaction mass spectrometry de Gouw, Joost; Warneke, Carsten Mass Spectrometry Reviews, Vol. 26, Issue 2 https://doi.org/10.1002/mas.20119	journal	January 2007
ggplot2 Wickham, Hadley Springer New York, NY https://doi.org/10.1007/978-0-387-98141-3	book	January 2009
A global analysis of root distributions for terrestrial biomes Jackson, R. B.; Canadell, J.; Ehleringer, J. R. Oecologia, Vol. 108, Issue 3 https://doi.org/10.1007/BF00333714	journal	November 1996
Quantitative measurement of food selection: A modification of the forage ratio and Ivlev's electivity index Jacobs, J�rgen Oecologia, Vol. 14, Issue 4 https://doi.org/10.1007/BF00384581	journal	January 1974
Detection of hypogeous fungi by Tasmanian bettong (Bettongia gaimardi: Marsupialia; Macropodoidea) Donaldson, Rebecca; Stoddart, Michael Journal of Chemical Ecology, Vol. 20, Issue 5 https://doi.org/10.1007/BF02059754	journal	May 1994
Sulfur volatiles of microbial origin are key contributors to human-sensed truffle aroma Splivallo, Richard; Ebeler, Susan E. Applied Microbiology and Biotechnology, Vol. 99, Issue 6 https://doi.org/10.1007/s00253-014-6360-9	journal	January 2015
Floral scent emission and pollinator attraction in two species of Gymnadenia (Orchidaceae) Huber, Franz K.; Kaiser, Roman; Sauter, Willi Oecologia, Vol. 142, Issue 4 https://doi.org/10.1007/s00442-004-1750-9	journal	December 2004
Use of digital webcam images to track spring green-up in a deciduous broadleaf forest Richardson, Andrew D.; Jenkins, Julian P.; Braswell, Bobby H. Oecologia, Vol. 152, Issue 2 https://doi.org/10.1007/s00442-006-0657-z	journal	March 2007
Controls of nitrogen isotope patterns in soil profiles Hobbie, Erik A.; Ouimette, Andrew P. Biogeochemistry, Vol. 95, Issue 2-3 https://doi.org/10.1007/s10533-009-9328-6	journal	May 2009
Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds Cazetta, Eliana; Schaefer, Hinrich Martin; Galetti, Mauro Evolutionary Ecology, Vol. 23, Issue 2 https://doi.org/10.1007/s10682-007-9217-1	journal	October 2007
Plant attractants: integrating insights from pollination and seed dispersal ecology Valenta, Kim; Nevo, Omer; Martel, Carlos Evolutionary Ecology, Vol. 31, Issue 2 https://doi.org/10.1007/s10682-016-9870-3	journal	October 2016
Interactions between mammals and ectomycorrhizal fungi Johnson, Christopher N. Trends in Ecology & Evolution, Vol. 11, Issue 12 https://doi.org/10.1016/S0169-5347(96)10053-7	journal	December 1996
Dimethyl sulphide: the secret for black truffle hunting by animals? Talou, T.; Gaset, A.; Delmas, M. Mycological Research, Vol. 94, Issue 2 https://doi.org/10.1016/S0953-7562(09)80630-8	journal	March 1990
Nitrogen content, amino acid composition and digestibility of fungi from a nutritional perspective in animal mycophagy Wallis, Ian R.; Claridge, Andrew W.; Trappe, James M. Fungal Biology, Vol. 116, Issue 5 https://doi.org/10.1016/j.funbio.2012.02.007	journal	May 2012
Gut-retention time in mycophagous mammals: a review and a study of truffle-like fungal spore retention in the swamp wallaby Danks, Melissa A. Fungal Ecology, Vol. 5, Issue 2 https://doi.org/10.1016/j.funeco.2011.08.005	journal	April 2012
Drivers of truffle biomass, community composition, and richness among forest types in the northeastern US Stephens, Ryan B.; Remick, Tyler J.; Ducey, Mark J. Fungal Ecology, Vol. 29 https://doi.org/10.1016/j.funeco.2017.05.004	journal	October 2017
Volatile compounds from six species of truffle – head-space analysis and vapor analysis at high mass resolution March, Raymond E.; Richards, Don S.; Ryan, Robert W. International Journal of Mass Spectrometry, Vol. 249-250 https://doi.org/10.1016/j.ijms.2005.12.038	journal	March 2006
Controls of isotopic patterns in saprotrophic and ectomycorrhizal fungi Hobbie, Erik A.; Sánchez, Fernando S.; Rygiewicz, Paul T. Soil Biology and Biochemistry, Vol. 48 https://doi.org/10.1016/j.soilbio.2012.01.014	journal	May 2012
Proton-Transfer Reaction Mass Spectrometry Blake, Robert S.; Monks, Paul S.; Ellis, Andrew M. Chemical Reviews, Vol. 109, Issue 3 https://doi.org/10.1021/cr800364q	journal	March 2009
Accelerated evolution of a false-truffle from a mushroom ancestor Bruns, Thomas D.; Fogel, Robert; White, Thomas J. Nature, Vol. 339, Issue 6220 https://doi.org/10.1038/339140a0	journal	May 1989
Environmental conditions influence the biochemical properties of the fruiting bodies of Tuber magnatum Pico Vita, Federico; Franchina, Flavio Antonio; Taiti, Cosimo Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-25520-7	journal	May 2018
Colour and odour drive fruit selection and seed dispersal by mouse lemurs Valenta, Kim; Burke, Ryan J.; Styler, Sarah A. Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep02424	journal	August 2013
Proton-transfer-reaction mass spectrometry (PTR–MS): on-line monitoring of volatile organic compounds at pptv levels Lindinger, W.; Jordan, A. Chemical Society Reviews, Vol. 27, Issue 5 https://doi.org/10.1039/a827347z	journal	January 1998
Australian species of Elaphomyces (Elaphomycetaceae, Eurotiales, Ascomycota) Castellano, Michael A.; Trappe, James M.; Vernes, Karl Australian Systematic Botany, Vol. 24, Issue 1 https://doi.org/10.1071/SB10012	journal	January 2011
Dispersers shape fruit diversity in Ficus (Moraceae) Lomascolo, S. B.; Levey, D. J.; Kimball, R. T. Proceedings of the National Academy of Sciences, Vol. 107, Issue 33 https://doi.org/10.1073/pnas.1008773107	journal	August 2010
Variations of Box Plots Mcgill, Robert; Tukey, John W.; Larsen, Wayne A. The American Statistician, Vol. 32, Issue 1 https://doi.org/10.1080/00031305.1978.10479236	journal	February 1978
Lessons from Alpine Fungi Trappe, James M. Mycologia, Vol. 80, Issue 1 https://doi.org/10.1080/00275514.1988.12025490	journal	January 1988
Sequestrate fungi of New Zealand: Elaphomyces (Ascomycota, Eurotiales, Elaphomycetaceae) Castellano, Michael A.; Beever, Ross E.; Trappe, James M. New Zealand Journal of Botany, Vol. 50, Issue 4 https://doi.org/10.1080/0028825X.2012.725057	journal	December 2012
Converting Nitrogen into Protein—Beyond 6.25 and Jones' Factors Mariotti, François; Tomé, Daniel; Mirand, Philippe Patureau Critical Reviews in Food Science and Nutrition, Vol. 48, Issue 2 https://doi.org/10.1080/10408390701279749	journal	January 2008
2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education: Sikes, Robert S. Journal of Mammalogy, Vol. 97, Issue 3 https://doi.org/10.1093/jmammal/gyw078	journal	May 2016
Bacteria associated with truffle-fruiting bodies contribute to truffle aroma: Bacteria produce truffle volatiles Splivallo, Richard; Deveau, Aurélie; Valdez, Nayuf Environmental Microbiology, Vol. 17, Issue 8 https://doi.org/10.1111/1462-2920.12521	journal	July 2014
Fine-scale spatial genetic structure analysis of the black truffle T uber aestivum and its link to aroma variability : Tuber aestivum: genetic and aroma variability Molinier, Virginie; Murat, Claude; Frochot, Henri Environmental Microbiology, Vol. 17, Issue 8 https://doi.org/10.1111/1462-2920.12910	journal	July 2015
Plant odour plumes as mediators of plant-insect interactions: Plant odour plumes Beyaert, Ivo; Hilker, Monika Biological Reviews, Vol. 89, Issue 1 https://doi.org/10.1111/brv.12043	journal	May 2013
Synchrony in small mammal community dynamics across a forested landscape Stephens, Ryan B.; Hocking, Daniel J.; Yamasaki, Mariko Ecography, Vol. 40, Issue 10 https://doi.org/10.1111/ecog.02233	journal	November 2016
Bees use honest floral signals as indicators of reward when visiting flowers Knauer, A. C.; Schiestl, F. P. Ecology Letters, Vol. 18, Issue 2 https://doi.org/10.1111/ele.12386	journal	December 2014
Birds use fruit colour as honest signal of dietary antioxidant rewards Schaefer, H. M.; McGraw, K.; Catoni, C. Functional Ecology, Vol. 22, Issue 2 https://doi.org/10.1111/j.1365-2435.2007.01363.x	journal	April 2008
Role of odour compounds in the attraction of gamete vectors in endophytic Epichloë fungi Steinebrunner, Fabrizio; Twele, Robert; Francke, Wittko New Phytologist, Vol. 178, Issue 2 https://doi.org/10.1111/j.1469-8137.2007.02347.x	journal	January 2008
Truffle volatiles: from chemical ecology to aroma biosynthesis: Research review Splivallo, Richard; Ottonello, Simone; Mello, Antonietta New Phytologist, Vol. 189, Issue 3 https://doi.org/10.1111/j.1469-8137.2010.03523.x	journal	November 2010
Fruit aromas in mature fleshy fruits as signals of readiness for predation and seed dispersal Rodríguez, Ana; Alquézar, Berta; Peña, Leandro New Phytologist, Vol. 197, Issue 1 https://doi.org/10.1111/j.1469-8137.2012.04382.x	journal	November 2012
Fungal functioning in a pine forest: evidence from a ¹⁵ N-labeled global change experiment Hobbie, Erik A.; van Diepen, Linda T. A.; Lilleskov, Erik A. New Phytologist, Vol. 201, Issue 4 https://doi.org/10.1111/nph.12578	journal	November 2013
Competitive avoidance not edaphic specialization drives vertical niche partitioning among sister species of ectomycorrhizal fungi Mujic, Alija B.; Durall, Daniel M.; Spatafora, Joseph W. New Phytologist, Vol. 209, Issue 3 https://doi.org/10.1111/nph.13677	journal	September 2015
Mechanisms of truffle detection by northern flying squirrels Pyare, Sanjay; Longland, William S. Canadian Journal of Zoology, Vol. 79, Issue 6 https://doi.org/10.1139/z01-069	journal	June 2001
Signals Can Trump Rewards in Attracting Seed-Dispersing Ants Turner, Kyle M.; Frederickson, Megan E. PLoS ONE, Vol. 8, Issue 8 https://doi.org/10.1371/journal.pone.0071871	journal	August 2013
Why Do Floral Perfumes Become Different? Region-Specific Selection on Floral Scent in a Terrestrial Orchid Gross, Karin; Sun, Mimi; Schiestl, Florian P. PLOS ONE, Vol. 11, Issue 2 https://doi.org/10.1371/journal.pone.0147975	journal	February 2016
Species Assemblages and Indicator Species:The need for a Flexible Asymmetrical Approach Dufrêne, Marc; Legendre, Pierre Ecological Monographs, Vol. 67, Issue 3 https://doi.org/10.1890/0012-9615(1997)067[0345:SAAIST]2.0.CO;2	journal	August 1997
Standing crop and Animal Consumption of Fungal Sporocarps in Pacific Northwest Forests North, Malcolm; Trappe, James; Franklin, Jerry Ecology, Vol. 78, Issue 5 https://doi.org/10.1890/0012-9658(1997)078[1543:SCAACO]2.0.CO;2	journal	July 1997
Reliable cues and signals of fruit quality are contingent on the habitat in black elder ( Sambucus nigra ) Schaefer, H. Martin; Braun, Julius Ecology, Vol. 90, Issue 6 https://doi.org/10.1890/08-1346.1	journal	June 2009
Associations between species and groups of sites: indices and statistical inference Cáceres, Miquel De; Legendre, Pierre Ecology, Vol. 90, Issue 12 https://doi.org/10.1890/08-1823.1	journal	December 2009
Site fidelity by bees drives pollination facilitation in sequentially blooming plant species Ogilvie, Jane E.; Thomson, James D. Ecology, Vol. 97, Issue 6 https://doi.org/10.1890/15-0903.1	journal	June 2016
Rates of Gut Passage and Retention of Hypogeous Fungal Spores in Two Forest-Dwelling Rodents Cork, S. J.; Kenagy, G. J. Journal of Mammalogy, Vol. 70, Issue 3 https://doi.org/10.2307/1381423	journal	August 1989
Measuring Preference in Selective Predation Chesson, Jean Ecology, Vol. 59, Issue 2 https://doi.org/10.2307/1936364	journal	March 1978
Fungal-Small Mammal Interrelationships with Emphasis on Oregon Coniferous Forests Maser, Chris; Trappe, James M.; Nussbaum, Ronald A. Ecology, Vol. 59, Issue 4 https://doi.org/10.2307/1938784	journal	July 1978
Nutritional Value of Hypogeous Fungus for a Forest-Dwelling Ground Squirrel Cork, S. J.; Kenagy, G. J. Ecology, Vol. 70, Issue 3 https://doi.org/10.2307/1940209	journal	June 1989
Multiple origins of sequestrate fungi related to Cortinarius (Cortinariaceae) Peintner, Ursula; Bougher, Neale L.; Castellano, Michael A. American Journal of Botany, Vol. 88, Issue 12 https://doi.org/10.2307/3558378	journal	December 2001
The Secotioid Syndrome Thiers, Harry D. Mycologia, Vol. 76, Issue 1 https://doi.org/10.2307/3792830	journal	January 1984
Lessons from Alpine Fungi Trappe, James M. Mycologia, Vol. 80, Issue 1 https://doi.org/10.2307/3807486	journal	January 1988
Three new black Elaphomyces species ( Elaphomycetaceae, Eurotiales, Ascomycota ) from eastern North America with notes on selected European species Castellano, M. A.; Elliott, T. F.; Trappe, J. M. Fungal Systematics and Evolution, Vol. 1, Issue 1 https://doi.org/10.3114/fuse.2018.01.01	journal	June 2018
The genus Elaphomyces ( Ascomycota, Eurotiales ): a ribosomal DNA-based phylogeny and revised systematics of European 'deer truffles' Paz, A.; Bellanger, J. -M.; Lavoise, C. Persoonia - Molecular Phylogeny and Evolution of Fungi, Vol. 38, Issue 1 https://doi.org/10.3767/003158517X697309	journal	June 2017
Convergent evolution of sequestrate forms in Amanita under Mediterranean climate conditions Justo, Alfredo; Morgenstern, Ingo; Hallen-Adams, Heather E. Mycologia, Vol. 102, Issue 3 https://doi.org/10.3852/09-191	journal	May 2010
Bees use honest floral signals as indicators of reward when visiting flowers Knauer, Anina C.; Schiestl, Florian P. Wiley-Blackwell Publishing, Inc. https://doi.org/10.5167/uzh-108858	text	January 2015
Role of odour compounds in the attraction of gamete vectors in endophytic Epichloë fungi Steinebrunner, F.; Twele, R.; Francke, W. Wiley-Blackwell https://doi.org/10.5167/uzh-11873	text	January 2008
Why do floral perfumes become different? Region-specific selection on floral scent in a terrestrial Orchid Gross, Karin; Sun, Mimi; Schiestl, Florian P. Public Library of Science (PLoS) https://doi.org/10.5167/uzh-123619	text	January 2016
New species of Elaphomyces (Elaphomycetaceae, Eurotiales, Ascomycota) from tropical rainforests of Cameroon and Guyana Castellano, Michael A.; Dentinger, Bryn T. M.; Séné, Olivier IMA Fungus, Vol. 7, Issue 1 https://doi.org/10.5598/imafungus.2016.07.01.05	journal	March 2016
Elaphomyces species (Elaphomycetaceae, Eurotiales) from Bartlett Experimental Forest, New Hampshire, USA Castellano, Michael A.; Stephens, Ryan B. IMA Fungus, Vol. 8, Issue 1 https://doi.org/10.5598/imafungus.2017.08.01.04	journal	March 2017
Associations between species and groups of sites: indices and statistical inference Cáceres, Miquel De; Legendre, Pierre Figshare https://doi.org/10.6084/m9.figshare.c.3301754	collection	January 2016

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54 ENVIRONMENTAL SCIENCES
Elaphomyces
chemical ecology
communication
environmental sciences & ecology
fungal interactions
fungal volatiles
fungivory
mammal
truffle
volatile organic compounds

Title: Signaling from below: rodents select for deeper fruiting truffles with stronger volatile emissions

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