Advertisement

Vegetation History and Archaeobotany

, Volume 28, Issue 1, pp 93–104 | Cite as

Dung fungi as a proxy for megaherbivores: opportunities and limitations for archaeological applications

  • Angelina G. PerrottiEmail author
  • Eline van Asperen
Review

Abstract

The use of spores of coprophilous fungi from sedimentary sequences as proxy evidence for large herbivore abundance has garnered pronounced attention and scrutiny over the past three decades. In response to the rapid rate at which new information is being discovered on this topic, this paper presents a brief review of the archaeological applications so far, and outlines opportunities and limitations of using Sporormiella as a proxy for herbivore abundance. Specific archaeological uses of this proxy include understanding megaherbivore extinctions and human land use patterns such as pastoralism and agriculture. We analyse how dung fungal records are formed and review the mycological literature to outline factors affecting spore reproduction and preservation. These include how strongly each commonly used dung fungal taxon relies on dung as a substrate and environmental factors affecting dung fungal reproduction and coprophilous fungi deposition. Certain laboratory preparation techniques adversely affect spore representation on pollen slides. The methods of analysis and quantification of spore records also impact our understanding. We describe good practice to increase precision of analytical methods. Due to limitations imposed by some of these factors, it is possible that an absence of dung fungi from a palaeoecological record does not imply an absence of herbivores. However, consideration of these factors and inclusion of as wide a range of coprophilous spore records as possible increases the reliability of such inferences.

Keywords

Coprophilous fungi Sporormiella Palynology Megafaunal extinction Pastoral activity NPP 

Notes

Acknowledgements

Thank you to Chase Beck for creating Fig. 1 in this manuscript. We are appreciative of Bas van Geel and an anonymous reviewer for providing feedback that improved the quality of this manuscript. Many additional thanks to Vaughn Bryant for providing helpful feedback on many early iterations of this paper.

References

  1. Ahlborn M, Haberzettl T, Wang J et al (2015) Sediment dynamics and hydrologic events affecting small lacustrine systems on the southern-central Tibetan Plateau—the example of TT lake. Holocene 25:508–522Google Scholar
  2. Ahmed SI, Cain R (1972) Revision of the genera Sporormia and Sporormiella. Can J Bot 50:419–477Google Scholar
  3. Alroy J (2001) A multispecies overkill simulation of the end-pleistocene megafaunal mass extinction. Science 292:1,893–1,896.  https://doi.org/10.1126/science.1059342 Google Scholar
  4. Angel SK, Wicklow DT (1983) Coprophilous fungal communities in semiarid to mesic grasslands. Can J Bot 61:594–602.  https://doi.org/10.1139/b83-067 Google Scholar
  5. Asina S, Jain K, Cain RF (1977) Factors influencing ascospore germination in three species of Sporormiella. Can J Bot 55:1,908–1,914.  https://doi.org/10.1139/b77-218 Google Scholar
  6. Baker AG, Bhagwat SA, Willis KJ (2013) Do spores of coprophilous fungi make a good proxy for past distribution of large herbivores? Quat Sci Rev 62:21–31.  https://doi.org/10.1016/j.quascirev.2012.11.018 Google Scholar
  7. Baker AG, Cornelissen P, Bhagwat SA et al (2016) Quantification of population sizes of large herbivores and their long-term functional role in ecosystems using spores of coprophilous fungi. Methods Ecol Evol 7:1,273-1,281.  https://doi.org/10.1111/2041-210X.12580 Google Scholar
  8. Barr ME (2000) Notes on coprophilous bitunicate ascomycetes. Mycotaxon 76:105–112Google Scholar
  9. Bell A (1983) Dung fungi: an illustrated guide to coprophilous fungi in New Zealand. Victoria University Press, WellingtonGoogle Scholar
  10. Bell A (2005) An illustrated guide to coprophilous fungi Ascomycetes of Australia. CBS biodiversity series, vol 3. Centraalbureau voor Schimmelcultures, UtrechtGoogle Scholar
  11. Bertone M, Green J, Washburn S et al (2005) Seasonal activity and species composition of dung beetles (Coleoptera: Scarabaeidae and Geotrupidae) inhabiting cattle pastures in North Carolina. Ann Entomol Soc Am 98:309–321. https://doi.org/10.1603/0013-8746(2005)098[0309:SAASCO]2.0.CO;2Google Scholar
  12. Beynon SA (2012) Potential environmental consequences of administration of anthelmintics to sheep. Vet Parasitol 189:113–124.  https://doi.org/10.1016/j.vetpar.2012.03.040 Google Scholar
  13. Burney D, Robinson GS, Burney LP (2003) Sporormiella and the late Holocene extinctions in Madagascar. Proc Natl Acad Sci 100:10,800–10,805.  https://doi.org/10.1073/pnas.1534700100 Google Scholar
  14. Cain RF (1961) Studies of coprophilous ascomycetes. VII: Preussia. Can J Bot 39:1,633–1,666Google Scholar
  15. Clarke CM (1994) Differential recovery of fungal and algal palynomorphs versus embryophyte pollen and spores by three processing techniques. In: Davis OK (ed) Aspects of archaeological palynology: methodology and applications. American Association of Stratigraphic Palynologists, College Station, pp 53–62Google Scholar
  16. Cugny C, Mazier F, Galop D (2010) Modern and fossil non-pollen palynomorphs from the Basque mountains (western Pyrenees, France): the use of coprophilous fungi to reconstruct pastoral activity. Veget Hist Archaeobot 19:391–408.  https://doi.org/10.1007/s00334-010-0242-6 Google Scholar
  17. Davis ALV (1994) Compositional differences between dung beetle (Coleoptera: Scarabaeidae s. str.) assemblages in winter and summer rainfall climates. Afr Entomol 2:45–51Google Scholar
  18. Davis OK (1987) Spores of the dung fungus Sporormiella: increased abundance in historic sediments and before Pleistocene megafaunal extinction. Quat Res 28:290–294.  https://doi.org/10.1016/0033-5894(87)90067-6 Google Scholar
  19. Davis OK, Shafer DS (2006) Sporormiella fungal spores, a palynological means of detecting herbivore density. Palaeogeogr Palaeoclimatol Palaeoecol 237:40–50.  https://doi.org/10.1016/j.palaeo.2005.11.028 Google Scholar
  20. Deacon J (2006) Fungal biology. Blackwell Publishing, MaldenGoogle Scholar
  21. Dickinson CH, Underhay VHS (1977) Growth of fungi in cattle dung. Trans Br Mycol Soc 69:473–477.  https://doi.org/10.1016/S0007-1536(77)80086-7 Google Scholar
  22. Dix NJ, Webster J (1995) Fungal ecology. Springer, DordrechtGoogle Scholar
  23. Doveri F (2007) Fungi Fimicoli Italici. Associazione Micologica Bresadola/Fondazione Centro Studio Micologici Dell’A.M.B, TrentoGoogle Scholar
  24. Doyen E, Etienne D (2017) Ecological and human land-use indicator value of fungal spore morphotypes and assemblages. Veget Hist Archaeobot 26:357–367.  https://doi.org/10.1007/s00334-016-0599-2 Google Scholar
  25. Ebersohn C, Eicker A (1992) Coprophilous fungal species composition and species diversity on various dung substrates of African game animals. Bot Bull Acad Sin 33:85–95Google Scholar
  26. Edwards PB (1991) Seasonal variation in the dung of African grazing mammals, and its consequences for coprophagous insects. Funct Ecol 5:617–628.  https://doi.org/10.2307/2389480 Google Scholar
  27. Etienne D, Jouffroy-Bapicot I (2014) Optimal counting limit for fungal spore abundance estimation using Sporormiella as a case study. Veget Hist Archaeobot 23:743–749.  https://doi.org/10.1007/s00334-014-0439-1 Google Scholar
  28. Etienne D, Wilhelm B, Sabatier P, Reyss J-L, Arnaud F (2013) Influence of sample location and livestock numbers on Sporormiella concentrations and accumulation rates in surface sediments of Lake Allos, French Alps. J Paleolimnol 49:117–127.  https://doi.org/10.1007/s10933-012-9646-x Google Scholar
  29. Fægri K, Iversen J (1989) Textbook of pollen analysis, 4th edn., edited by Fægri K, Kaland PE, Krzywinski K. Wiley, ChichesterGoogle Scholar
  30. Feeser I, O’Connell M (2010) Late Holocene land-use and vegetation dynamics in an upland karst region based on pollen and coprophilous fungal spore analyses: an example from the Burren, western Ireland. Veget Hist Archaeobot 19:409–426.  https://doi.org/10.1007/s00334-009-0235-5 Google Scholar
  31. Felauer T, Schlütz F, Murad W, Mischke S, Lehmkuhl F (2012) Late quaternary climate and landscape evolution in arid Central Asia: a multiproxy study of lake archive Bayan Tohomin Nuur, Gobi Desert, southern Mongolia. J Asian Earth Sci 48:125–135Google Scholar
  32. Fiedel SJ (2018) The spore conundrum: does a dung fungus decline signal humans’ arrival in the Eastern United States? Quat Int 466(b):247–255.  https://doi.org/10.1016/j.quaint.2015.11.130 Google Scholar
  33. Firestone RB, West A, Kennett JP et al (2007) Evidence for an extraterrestrial impact 12,900 years ago that contributed to the megafaunal extinctions and the Younger Dryas cooling. Proc Natl Acad Sci 104:16,016–16,021.  https://doi.org/10.1073/pnas.0706977104 Google Scholar
  34. Floate KD, Gill BD (1998) Seasonal activity of dung beetles (Coleoptera: Scarabaeidae) associated with dung in Southern Alberta and their geographic distribution in Canada. Can Entomol 130:131–151.  https://doi.org/10.4039/Ent130131-2 Google Scholar
  35. Frank M, Slaton A, Tinta T, Capaldi A (2015) Investigating anthropogenic mammoth extinction with mathematical models. Spora J Biomath 1:8–16Google Scholar
  36. Gelorini V, Verbeken A, van Geel B et al (2011) Modern non-pollen palynomorphs from East African lake sediments. Rev Palaeobot Palynol 164:143–173.  https://doi.org/10.1016/j.revpalbo.2010.12.002 Google Scholar
  37. Ghosh R, Paruya DK, Acharya K et al (2017) How reliable are non-pollen palynomorphs in tracing vegetation changes and grazing activities? Study from the Darjeeling Himalaya, India. Palaeogeogr Palaeoclimatol Palaeoecol 475:23–40.  https://doi.org/10.1016/j.palaeo.2017.03.006 Google Scholar
  38. Gill JL (2014) Ecological impacts of the late quaternary megaherbivore extinctions. New Phytol 201:1,163–1,169.  https://doi.org/10.1111/nph.12576 Google Scholar
  39. Gill JL, McLauchlan KK, Skibbe AM et al (2013) Linking abundances of the dung fungus Sporormiella to the density of bison: implications for assessing grazing by megaherbivores in palaeorecords. J Ecol 101:1,125–1,136.  https://doi.org/10.1111/1365-2745.12130 Google Scholar
  40. Gill JL, Williams JW, Jackson ST et al (2009) Pleistocene megafaunal collapse, novel plant communities, and enhanced fire regimes in North America. Science 326:1,100–1,103.  https://doi.org/10.1126/science.1179504 Google Scholar
  41. Gill JL, Williams JW, Jackson ST, Donnelly JP, Schellinger GC (2012) Climatic and megaherbivory controls on late-glacial vegetation dynamics: a new, high-resolution, multi-proxy record from Silver Lake, Ohio. Quat Sci Rev 34:66–80Google Scholar
  42. Graf M-T, Chmura GL (2006) Development of modern analogues for natural, mowed and grazed grasslands using pollen assemblages and coprophilous fungi. Rev Palaeobot Palynol 141:139–149.  https://doi.org/10.1016/j.revpalbo.2006.03.018 Google Scholar
  43. Graham RW, Belmecheri S, Choy K et al (2016) Timing and causes of mid-Holocene mammoth extinction on St. Paul Island, Alaska. Proc Natl Acad Sci 113:9,310–9,314.  https://doi.org/10.1073/pnas.1604903113 Google Scholar
  44. Grayson DK, Meltzer DJ (2003) A requiem for North American overkill. J Archaeol Sci 30:585–593Google Scholar
  45. Greenham PM (1972) The effects of the variability of cattle dung on the multiplication of the bushfly (Musca vetustissima Walk.). J Anim Ecol 41:153–165.  https://doi.org/10.2307/3510 Google Scholar
  46. Guarro J, Gené J, Stchigel AM, Figueras MJ (2012) Atlas of soil ascomycetes. CBS-KNAW Fungal Biodiversity Centre, UtrechtGoogle Scholar
  47. Guthrie RD (1984) Alaskan megabucks, megabulls, and megarams: the issue of Pleistocene gigantism. Spec Publ Carnegie Mus Nat History 8:482–509Google Scholar
  48. Halligan JJ, Waters MR, Perrotti A et al (2016) Pre-Clovis occupation 14,550 years ago at the Page-Ladson site, Florida, and the peopling of the Americas. Sci Adv 2:e1600375–e1600375.  https://doi.org/10.1126/sciadv.1600375 Google Scholar
  49. Hanlin RT (1990) Illustrated genera of ascomycetes, vols I and II. The American Phytopatholocial Society, St. PaulGoogle Scholar
  50. Harper JE, Webster J (1964) An experimental analysis of the coprophilous fungus succession. Trans Br Mycol Soc 47:511–530.  https://doi.org/10.1016/S0007-1536(64)80029-2 Google Scholar
  51. Harrower KM, Nagy LA (1979) Effects of nutrients and water stress on growth and sporulation of coprophilous fungi. Trans Br Mycol Soc 72:459–462.  https://doi.org/10.1016/S0007-1536(79)80154-0 Google Scholar
  52. Hockett B (2005) Middle and late holocene hunting in the Great Basin: a critical review of the debate and future prospects. Am Antiqu 70:713–731.  https://doi.org/10.2307/40035871 Google Scholar
  53. Hockett B, Murphy TW (2009) Antiquity of communal pronghorn hunting in the North-Central Great Basin. Am Antiqu 74:708–734.  https://doi.org/10.1017/S0002731600049027 Google Scholar
  54. Ingold CT (1961) Ballistics in certain ascomycetes. New Phytol 60:143–149.  https://doi.org/10.1111/j.1469-8137.1961.tb06248.x Google Scholar
  55. Ingold CT, Hadland SA (1959) The ballistics of Sordaria. New Phytol 58:46–57.  https://doi.org/10.1111/j.1469-8137.1959.tb05333.x Google Scholar
  56. Janczewski E (1871) Morphologische untersuchungen über Ascobolus furfuraceus. Bot Z 29:271–279Google Scholar
  57. Johnson CN, Rule S, Haberle SG et al (2015) Using dung fungi to interpret decline and extinction of megaherbivores: problems and solutions. Quat Sci Rev 110:107–113.  https://doi.org/10.1016/j.quascirev.2014.12.011 Google Scholar
  58. Jones RA, Williams JW, Jackson ST (2017) Vegetation history since the last glacial maximum in the Ozark highlands (USA): a new record from Cupola Pond, Missouri. Quat Sci Rev 170:174–187Google Scholar
  59. Kadiri N, Lumaret J-P, Floate KD (2014) Functional diversity and seasonal activity of dung beetles (Coleoptera: Scarabaeoidea) on native grasslands in southern Alberta. Canada Can Entomol 146:291–305.  https://doi.org/10.4039/tce.2013.75 Google Scholar
  60. Kamerling IM, Schofield JE, Edwards KJ, Aronsson K-Å (2017) High-resolution palynology reveals the land use history of a Sami renvall in northern Sweden. Veget Hist Archaeobot 26:369–388.  https://doi.org/10.1007/s00334-016-0596-5 Google Scholar
  61. Krug JC, Benny GL, Keller HW (2004) Coprophilous fungi. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi, inventory and monitoring methods. Elsevier, Burlington, pp 467–499Google Scholar
  62. Krug JC, Udagawa S, Jeng RS (1983) The genus Apiosordaria. Mycotaxon 17:533–549Google Scholar
  63. Kruys Å, Wedin M (2009) Phylogenetic relationships and an assessment of traditionally used taxonomic characters in the Sporormiaceae (Pleosporales, Dothideomycetes, Ascomycota), utilising multi-gene phylogenies. Syst Biodivers 7:465–478.  https://doi.org/10.1017/S1477200009990119 Google Scholar
  64. Kuthubutheen AJ, Webster J (1986a) Effects of water availability on germination, growth and sporulation of coprophilous fungi. Trans Br Mycol Soc 86:77–91.  https://doi.org/10.1016/S0007-1536(86)80119-X Google Scholar
  65. Kuthubutheen AJ, Webster J (1986b) Water availability and the coprophilous fungus succession. Trans Br Mycol Soc 86:63–76.  https://doi.org/10.1016/S0007-1536(86)80118-8 Google Scholar
  66. Lehmkuhl F, Hilgers A, Fries S, Hülle D, Schlütz F, Shumilovskikh L, Felauer T, Protze J (2011) Holocene geomorphological processes and soil development as indicator for environmental change around Karakorum, Upper Orkhon Valley (Central Mongolia). Catena 87:31–44Google Scholar
  67. Lockwood JL (1977) Fungistasis in soils. Biol Rev 52:1–43.  https://doi.org/10.1111/j.1469-185X.1977.tb01344.x Google Scholar
  68. Lundqvist N (1972) Nordic Sordariaceae s. lat. Acta Universitas Upsaliensis. Symbolae Botanicae Uppsalienses, vol 20, 1. Acta Universitatis Upsaliensis, UppsalaGoogle Scholar
  69. Lussenhop J, Kumar R, Wicklow DT, Lloyd JE (1980) Insect effects on bacteria and fungi in Cattle Dung. Oikos 34:54.  https://doi.org/10.2307/3544549 Google Scholar
  70. Lussenhop J, Wicklow DT (1985) Interaction of competing fungi with fly larvae. Microb Ecol 11:175–182.  https://doi.org/10.1007/BF02010489 Google Scholar
  71. Macphee RDE (1997) The 40,000-year plague: humans, hyperdisease, and first-contact extinctions. In: Goodman SM, Patterson BD (eds) PattersonNatural change and human impact in Madagascar, 1st edn. Smithsonian Institution Scholarly Press, Washington DC, pp 169–217Google Scholar
  72. Martin PS (1984) Prehistoric overkill: the global model. In: Martin PS (ed) Quaternary extinctions: a prehistoric revolution. The University of Arizona Press, Tuscon, pp 354–403Google Scholar
  73. Massee G, Salmon ES (1902) Researches on coprophilous fungi, Vol II. Ann Bot 16:57–93Google Scholar
  74. Miehe G, Miehe S, Kaiser K, Reudenbach C, Behrendes L, Duo L, Schlütz F (2009) How old is pastoralism in Tibet? An ecological approach to the making of a Tibetan landscape. Palaeogeogr Palaeoclimatol Palaeoecol 276:130–147Google Scholar
  75. Moore PD, Webb JA, Collison ME (1991) Pollen analysis, 2nd edn. Blackwell Scientific, LondonGoogle Scholar
  76. Mungai P, Hyde KD, Cai L et al (2011) Coprophilous ascomycetes of northern Thailand. Curr Res Environ Appl Mycol 1:135–159Google Scholar
  77. Mungai PG, Njogu JG, Chukeatirote E, Hyde KD (2012) Coprophilous ascomycetes in Kenya: Sporormiella from wildlife dung. Mycology 3:234–251.  https://doi.org/10.1080/21501203.2012.752413 Google Scholar
  78. Newcombe G, Campbell J, Griffith D et al (2016) Revisiting the life cycle of dung fungi, including Sordaria fimicola. PloS One 11:e0147425Google Scholar
  79. Nyberg Å, Persson I-L (2002) Habitat differences of coprophilous fungi on moose dung. Mycol Res 106:1,360–1,366.  https://doi.org/10.1017/S0953756202006597 Google Scholar
  80. Omaliko CPE (1981) Dung deposition, breakdown and grazing behavior of beef cattle at two seasons in a tropical grassland ecosystem. J Range Manag 34:360–362.  https://doi.org/10.2307/3897903 Google Scholar
  81. Parker NE, Williams JW (2012) Influences of climate, cattle density, and lake morphology on Sporormiella abundances in modern lake sediments in the US Great Plains. Holocene 22:475–483Google Scholar
  82. Perrotti AG (2018) Pollen and Sporormiella evidence for terminal Pleistocene vegetation change and megafaunal extinction at Page-Ladson, Florida. Quat Int 466(b):256–268.  https://doi.org/10.1016/j.quaint.2017.10.015 Google Scholar
  83. Perrotti AG, Siskind T, Bryant MK, Bryant VM (2018) The efficacy of sonication-assisted sieving on quaternary pollen samples. Palynology.  https://doi.org/10.1080/01916122.2017.1394925 Google Scholar
  84. Piontelli E, Santa-Maria MAT, Caretta G (1981) Coprophilous fungi of the horse. Mycopathologia 74:89–105.  https://doi.org/10.1007/BF01259464 Google Scholar
  85. Ponel P, Court-Picon M, Guiter F, de Beaulieu JL, Andrieu-Ponel V, Djamali M, Leydet M, Gandouin E, Buttler A (2011) Holocene history of Lac des Lauzons (2180 m asl), reconstructed from multiproxy analyses of Coleoptera, plant macroremains and pollen (HautesAlpes, France). Holocene 21:565–582Google Scholar
  86. Raczka MF, Bush MB, Folcik AM, McMichael CH (2016) Sporormiella as a tool for detecting the presence of large herbivores in the Neotropics. Biota Neotrop.  https://doi.org/10.1590/1676-0611-BN-2015-0090 Google Scholar
  87. Raper D, Bush M (2009) A test of Sporormiella representation as a predictor of megaherbivore presence and abundance. Quat Res 71:490–496.  https://doi.org/10.1016/j.yqres.2009.01.010 Google Scholar
  88. Richardson MJ (1972) Coprophilous ascomycetes on different dung types. Trans Br Mycol Soc 58:37–48.  https://doi.org/10.1016/S0007-1536(72)80069-X Google Scholar
  89. Richardson MJ (2001) Diversity and occurrence of coprophilous fungi. Mycol Res 105:387–402.  https://doi.org/10.1017/S0953756201003884 Google Scholar
  90. Riding JB, Kyffin-Hughes JE (2004) A review of the laboratory preparation of Palynomorphs with a description of an effective non-acid technique. Revis Bras Paleontol 7:13–44Google Scholar
  91. Rule S, Brook BW, Haberle SG et al (2012) The aftermath of megafaunal extinction: ecosystem transformation in pleistocene Australia. Science 335:1,483–1,486.  https://doi.org/10.1126/science.1214261 Google Scholar
  92. Schlütz F, Shumilovskikh L (2017) Nonpollen palynomorphs notes: 1. Type HdV368 (Podospora-type), descriprions of associated species, and the first key to related spore types. Rev Palaeobot Palynol 239:47–54Google Scholar
  93. Shumilovskikh L, Djamali M, Andrieu-Ponel V, Ponel P, de Beaulieu JL, Naderi-Beni A, Sauer EW (2017) 3. Palaeoecological insights into agrihorticultural and pastoral practices before, during and after the Sasanian Empire. In: Sauer E (ed) Sasanian Persia: between Rome and the Steppes of Eurasia. Edinburgh University Press, Edinburgh, pp 51–73Google Scholar
  94. Shumilovskikh LS, Hopper K, Djamali M et al (2016a) Landscape evolution and agrosylvopastoral activities on the Gorgan Plain (NE Iran) in the last 6000 years. Holocene 26:1,676–1,691Google Scholar
  95. Shumilovskikh LS, Seeliger M, Feuser S et al (2016b) The harbour of Elaia: a palynological archive for human environmental interactions during the last 7500 years. Quat Sci Rev 149:167–187.  https://doi.org/10.1016/j.quascirev.2016.07.014 Google Scholar
  96. Surovell TA, Pelton SR, Anderson-Sprecher R, Myers AD (2016) Test of Martin’s overkill hypothesis using radiocarbon dates on extinct megafauna. Proc Natl Acad Sci 113:886–891.  https://doi.org/10.1073/pnas.1504020112 Google Scholar
  97. Surovell TA, Waguespack NM (2009) Human prey choice in the late Pleistocene and its relation to megafaunal extinctions. In: Haynes G (ed) American megafaunal extinctions at the end of the pleistocene. Springer, Netherlands, pp 77–105Google Scholar
  98. Szymanski RM (2017) Detection of human landscape alteration using nested microbotanical and fungal proxies. Environ Archaeol 22:434–446.  https://doi.org/10.1080/14614103.2017.1299415 Google Scholar
  99. Trail F (2007) Fungal cannons: explosive spore discharge in the Ascomycota. FEMS Microbiol Lett 276:12–18.  https://doi.org/10.1111/j.1574-6968.2007.00900.x Google Scholar
  100. Van Asperen EN (2017) Fungal diversity on dung of tropical animals in temperate environments: implications for reconstructing past megafaunal populations. Fungal Ecol 28:25–32.  https://doi.org/10.1016/j.funeco.2016.12.006 Google Scholar
  101. Van Asperen EN, Kirby JR, Hunt CO (2016) The effect of preparation methods on spores of coprophilous fungi: implications for recognition of megafaunal populations. Rev Palaeobot Palynol 229:1–8.  https://doi.org/10.1016/j.revpalbo.2016.02.004 Google Scholar
  102. Van der Kaars S, Miller GH, Turney CSM et al (2017) Humans rather than climate the primary cause of Pleistocene megafaunal extinction in Australia. Nat Commun 8:141–142Google Scholar
  103. Van Geel B, Buurman J, Brinkkemper O, Schelvis J, Aptroot A, van Reenen G, Hakbijl T (2003) Environmental reconstruction of a Roman period settlement site in Uitgeest (The Netherlands), with special reference to coprophilous fungi. J Archaeol Sci 30:873–883Google Scholar
  104. Van Geel B, Guthrie RD, Altmann JG et al (2011) Mycological evidence for coprophagy from the feces of an Alaskan Late Glacial mammoth. Quat Sci Rev 30:2,289–2,303Google Scholar
  105. Von Arx JA, van der Aa HA (1987) Spororminula tenerifae gen. et sp. nov. Trans Br Mycol Soc 89:117–120Google Scholar
  106. Wassmer T (2014) Seasonal occurrence (phenology) of coprophilous beetles (Coleoptera: Scarabaeidae and Hydrophilidae) from cattle and sheep farms in southeastern Michigan, USA. Coleopt Bull 68:603–618Google Scholar
  107. Webster J (1970) Coprophilous fungi. Trans Br Mycol Soc 54:161–180.  https://doi.org/10.1016/S0007-1536(70)80030-4 Google Scholar
  108. Wicklow DT (1992) The coprophilous fungal community: an experimental system. In: Carroll GC, Wicklow DT (eds) The fungal community: its organization and role in the ecosystem, 2nd edn. Marcel Dekker, New York, pp 715–728Google Scholar
  109. Wicklow DT, Angel K, Lussenhop J (1980) Fungal community expression in lagomorph versus ruminant feces. Mycologia 72:10–15.  https://doi.org/10.2307/3759740 Google Scholar
  110. Wicklow DT, Moore V (1974) Effect of incubation temperature on the coprophilous fungal succession. Trans Br Mycol Soc 62:411–415.  https://doi.org/10.1016/S0007-1536(74)80051-3 Google Scholar
  111. Wicklow DT, Yocom DH (1982) Effect of larval grazing by Lycoriella mali (Diptera:Sciaridae) on species abundance of coprophilous fungi. Trans Br Mycol Soc 78:29–32.  https://doi.org/10.1016/S0007-1536(82)80073-9 Google Scholar
  112. Wood JR, Wilmshurst JM (2013) Accumulation rates or percentages? How to quantify Sporormiella and other coprophilous fungal spores to detect late quaternary megafaunal extinction events. Quat Sci Rev 77:1–3Google Scholar
  113. Wood JR, Wilmshurst JM, Worthy TH, Cooper A (2011) Sporormiella as a proxy for non-mammalian herbivores in island ecosystems. Quat Sci Rev 30:915–920.  https://doi.org/10.1016/j.quascirev.2011.01.007 Google Scholar
  114. Yafetto L, Carroll L, Cui Y et al (2008) The fastest flights in nature: high-speed spore discharge mechanisms among fungi. PloS One 3:e3237.  https://doi.org/10.1371/journal.pone.0003237 Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of AnthropologyTexas A&M UniversityCollege StationUSA
  2. 2.Department of BiosciencesDurham UniversityDurhamUK
  3. 3.Department of AnthropologyDurham UniversityDurhamUK

Personalised recommendations