The management of the remainder of Europe’s once extensive forests is hampered by a poor understanding of the character of the vegetation and drivers of change before the onset of clearance for farming. Pollen data indicate a closed-canopy, mixed-deciduous forest, contrasting with the assertion that large herbivores would have maintained a mosaic of open grassland, regenerating scrub and forested groves. Coprophilous fungal spores from sedimentary sequences are increasingly used as a proxy for past herbivore impact on vegetation, but the method faces methodological and taphonomical issues. Using pollen trap data from a long-running experiment in Chillingham Wild Cattle Park, UK, we investigate the first steps in the mechanisms connecting herbivore density to the incorporation of fungal spores in sediments and assess the effects of environmental variables on this relationship. Herbivore utilisation levels correlate with dung fungal spore abundance. Chillingham is densely populated by large herbivores, but dung fungal spore influx is low. Herbivores may thus be present on the landscape but go undetected. The absence of dung fungal spores is therefore less informative than their presence. Dung fungal spores likely enter the sediment record through a different pathway from wind-borne pollen and thus dung fungal abundance is better expressed as influx rates than as percentage of total pollen. Landscape openness, vegetation type and site wetness do not distort the impact of utilisation levels on dung fungal spore representation. However, dung fungal spore influx varies markedly between seasons and years. Spores travel, leading to a background level of spore deposition across the landscape, and at times a depletion of spores, especially under wet weather conditions. Animal behaviour, as well as husbandry practices, can lead to the accumulation of dung, and thus fungal spores, in specific locations on the landscape that do not directly reflect grazing pressure.
BakerAGBhagwatSAWillisKJ (2013) Do dung fungal spores make a good proxy for past distribution of large herbivores?Quaternary Science Reviews62: 21–31.
2.
BakerAGCornelissenPBhagwatSA, et al. (2016) Quantification of population sizes of large herbivores and their long-term functional role in ecosystems using dung fungal spores. Methods in Ecology and Evolution7: 1273–1281.
3.
BasumatarySKMcDonaldHGGogoiR (2017) Pollen and non-pollen palynomorph preservation in the dung of the Greater One-horned Rhino (Rhinoceros unicornis), and its implication to palaeoecology and palaeodietary analysis: A case study from India. Review of Palaeobotany and Palynology244: 153–162.
4.
BellA (2005) An Illustrated Guide to the Coprophilous Ascomycetes of Australia (CBS Biodiversity Series No. 3). Utrecht: Fungal Biodiversity Centre.
5.
BirksHJB (2005) Mind the gap: How open were European primeval forests?Trends in Ecology and Evolution20: 154–156.
6.
BlackfordJJInnesJB (2006) Linking current environments and processes to fungal spore assemblages: Surface NMP data from woodland environments. Review of Palaeobotany and Palynology141: 179–187.
7.
BradshawRMitchellFJG (1999) The palaeoecological approach to reconstructing former grazing-vegetation interactions. Forest Ecology and Management120: 3–12.
8.
BradshawRHWHannonGEListerAM (2003) A long-term perspective on ungulate-vegetation interactions. Forest Ecology and Management181: 267–280.
9.
BridglandDRSchreveDCKeenDH, et al. (2004) Biostratigraphical correlation between the late Quaternary sequences of the Thames and key fluvial localities in central Germany. Proceedings of the Geologists’ Association115: 125–140.
10.
BroströmASugitaSGaillardMJ (2004) Pollen productivity estimates for the reconstruction of past vegetation cover in the cultural landscape of southern Sweden. The Holocene14: 368–381.
11.
BroströmANielsenABGaillardM-J, et al. (2008) Pollen productivity estimates of key European plant taxa for quantitative reconstruction of past vegetation: A review. Vegetation History and Archaeobotany17: 461–478.
12.
BucklandPC (2005) Palaeoecological evidence for the Vera hypothesis. In: HodderKHBullockJMBucklandPC, et al. (eds) Large Herbivores in the Wildwood and Modern Naturalistic Grazing Systems (English Nature Research Reports 648). Peterborough: English Nature, pp. 62–114.
13.
BunceRGHHallSJG (2013) Vegetation change from 1979 to 2008 at Chillingham Park in relation to conservation of the Chillingham Wild Cattle. Northumbrian Naturalist75: 18–30.
14.
CugnyCMazierFGalopD (2010) Modern and fossil non-pollen palynomorphs from the Basque mountains (western Pyrenees, France): The use of coprophilous fungi to reconstruct pastoral activity. Vegetation History and Archaeobotany19: 391–408.
15.
CurrantAPJacobiR (2010) The mammal faunas of the British Late Pleistocene. In: AshtonNMLewisSGStringerCB (eds) The Ancient Human Occupation of Britain (Developments in Quaternary Science 14). Amsterdam: Elsevier, pp. 165–180.
16.
DaviesAL (2016) Late Holocene regime shifts in moorland ecosystems: High resolution data from the Pennines, UK. Vegetation History and Archaeobotany25: 207–219.
17.
DavisOK (1987) Spores of the dung fungus Sporormiella: Increased abundance in historic sediments and before Pleistocene megafaunal extinction. Quaternary Research28: 290–294.
18.
DavisOKShaferDS (2006) Sporormiella fungal spores, a palynological means of detecting herbivore density. Palaeogeography, Palaeoclimatology, Palaeoecology237: 40–50.
19.
DietreBGauthierÉGilletF (2012) Modern pollen rain and fungal spore assemblages from pasture woodlands around Lake Saint-Point (France). Review of Palaeobotany and Palynology186: 69–89.
20.
DietreBWalserCKoflerW, et al. (2017) Neolithic to Bronze Age (4850-3450 cal. BP) fire management of the Alpine Lower Engadine landscape (Switzerland) to establish pastures and cereal fields. The Holocene27: 181–196.
21.
DoveriF (2007) Fungi Fimicoli Italici. Trento: Associazione Micologica Bresadola/Fondazione Centro Studio Micologici Dell’A.M.B.
22.
EkblomAGillsonL (2010) Dung fungi as indicators of past herbivore abundance, Kruger and Limpopo National Park. Palaeogeography, Palaeoclimatology, Palaeoecology296: 14–27.
23.
EtienneDJouffroy-BapicotI (2014) Optimal counting limit for fungal spore abundance estimation using Sporormiella as a case study. Vegetation History and Archaeobotany23: 743–749.
24.
EtienneDWilhelmBSabatierP, et al. (2013) Influence of sample location and livestock numbers on Sporormiella concentrations and accumulations rates in surface sediments of Lake Allos, French Alps. Journal of Paleolimnology49: 117–127.
25.
FaegriKIversenJ (1989) Textbook of Pollen Analysis. 4th Edition.Chichester: John Wiley & Sons.
26.
FeeserIDörflerW (2014) The glade effect: Vegetation openness and structure and their influences on arboreal pollen production and the reconstruction of anthropogenic forest opening. Anthropocene8: 92–100.
27.
FeeserIO’ConnellM (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. Vegetation History and Archaeobotany19: 409–426.
28.
FeranecRSMillerNGLothropJC, et al. (2011) The Sporormiella proxy and end-Pleistocene megafaunal extinction: A perspective. Quaternary International245: 333–338.
29.
ForbesTDAHodgsonJA (1985) The reaction of grazing sheep and cattle to the presence of dung from the same or the other species. Grass and Forage Science40: 177–182.
FyfeRMBrückJJohnstonR, et al. (2008) Historical context and chronology of Bronze Age land enclosure on Dartmoor, UK. Journal of Archaeological Science35: 2250–2261.
32.
FyfeRMTwiddleCSugitaS, et al. (2013) The Holocene vegetation cover of Britain and Ireland: Overcoming problems of scale and discerning patterns of openness. Quaternary Science Reviews73: 132–148.
33.
GhoshRParuyaDKAcharyaK, et al. (2017) How reliable are non-pollen palynomorphs in tracing vegetation changes and grazing activities? Study from the Darjeeling Himalaya, India. Palaeogeography, Palaeoclimatology, Palaeoecology475: 23–40.
34.
GillJL (2014) Ecological impacts of the late Quaternary megaherbivore extinctions. New Phytologist201: 1163–1169.
35.
GillJLMcLauchlanKKSkibbeAM, et al. (2013) Linking abundances of the dung fungus Sporormiella to the density of bison: Implications for assessing grazing by megaherbivores in palaeorecords. Journal of Ecology101: 1125–1136.
36.
GillJLWilliamsJWJacksonST, et al. (2009) Pleistocene megafaunal collapse, novel plant communities, and enhanced fire regimes in North America. Science326: 1100–1103.
37.
GillRMAMorganG (2010) The effects of varying deer density on natural regeneration in woodlands in lowland Britain. Forestry83: 53–63.
38.
GrafM-TChmuraGL (2006) Development of modern analogues for natural, mowed and grazed grasslands using pollen assemblages and coprophilous fungi. Review of Palaeobotany and Palynology141: 139–149.
39.
Groenman-van WaateringeW (1993) The effects of grazing on the pollen production of grasses. Vegetation History and Archaeobotany2: 157–162.
GuarroJGenéJStchigelAM, et al. (2012) Atlas of Soil Ascomycetes (CBS Biodiversity Series 10). Utrecht: CBS-KNAW Fungal Biodiversity Centre.
43.
HallSFletcherJGidlowJ, et al. (2005) Management of the Chillingham wild white cattle. Government Veterinary Journal15: 4–11.
44.
HallSJG (1988) Chillingham Park and its herd of white cattle: Relationships between vegetation classes and patterns of range use. Journal of Applied Ecology25: 777–789.
45.
HallSJG (2007) Chillingham wild cattle park, Northumberland. In: RotherhamID (ed.) The History, Ecology and Archaeology of Medieval Parks and Parklands (Landscape Archaeology and Ecology 6). Sheffield: Wildtrack Publishing, pp. 53–57.
46.
HallSJG (2013) Integrated conservation of a park and its associated cattle herd. In: RotherhamID (ed.) Trees, Forested Landscapes and Grazing Animals, a European Perspective on Woodlands and Grazed Treescapes. Abingdon: Routledge, pp. 242–254.
47.
HallSJGBunceRGH (1984) Vegetation survey of Chillingham Park, Northumberland. Transactions of the Natural History Society of Northumbria52: 5–14.
48.
HesterAJBergmanMIasonGR, et al. (2006) Impacts of large herbivores on plant community structure and dynamics. In: DanellKBergströmRDuncanP, et al. (eds) Large Herbivore Ecology, Ecosystem Dynamics and Conservation. Cambridge: Cambridge University Press, pp. 97–141.
49.
HicksS (2001) The use of annual arboreal pollen deposition values for delimiting tree-lines in the landscape and exploring models of pollen dispersal. Review of Palaeobotany and Palynology117: 1–29.
50.
HicksSHyvärinenV-P (1986) Sampling modern pollen deposition by means of ‘Tauber traps’: Some considerations. Pollen et Spores28: 219–242.
51.
HicksSAmmannBLatalowaM, et al. (1996) European Pollen Monitoring Programme, Project Description and Guidelines. Oulu: Oulu University Press.
52.
HicksSTinsleyHPardoeH, et al. (1999) European Pollen Monitoring Programme, Supplement to the Guidelines. Oulu: Oulu University Press.
53.
HodderKHBullockJM (2005a) Naturalistic grazing and conservation. In: HodderKHBullockJMBucklandPV, et al. (eds) Large Herbivores in the Wildwood and Modern Naturalistic Grazing Systems (English Nature Research Reports 648). Peterborough: English Nature, pp. 117–168.
54.
HodderKHBullockJM (2005b) The Vera model of post-glacial landscapes in Europe: A summary of the debate. In: HodderKHBullockJMBucklandPV, et al. (eds) Large Herbivores in the Wildwood and Modern Naturalistic Grazing Systems (English Nature Research Reports 648). Peterborough: English Nature, pp. 30–61.
55.
HumphreyJGillRClaridgeJ (1998) Grazing as a Management Tool in European Forest Ecosystems. Forestry Commission Technical Paper 25. Edinburgh: Forestry Commission.
56.
IngoldCT (1961) Ballistics in certain Ascomycetes. New Phytologist60: 143–149.
57.
IngoldCTHadlandSA (1959) The ballistics ofSordaria. New Phytologist58: 46–57.
58.
InnesJBBlackfordJJ (2003) The ecology of Late Mesolithic woodland disturbances: Model testing with fungal spore assemblage data. Journal of Archaeological Science30: 185–194.
59.
JacobsonGLBradshawRHW (1981) The selection of sites for paleovegetational studies. Quaternary Research16: 80–96.
JanssenCR (1967) A comparison between the recent regional pollen rain and the sub-recent vegetation in four major vegetation types in Minnesota (U.S.A.). Review of Palaeobotany and Palynology2: 331–342.
62.
JohnsonCNRuleSHaberleSG, et al. (2015) Using dung fungi to interpret decline and extinction of megaherbivores: Problems and solutions. Quaternary Science Reviews110: 107–113.
63.
JohnsonCNRuleSHaberleSG, et al. (2016) Geographic variation in the ecological effects of extinction of Australia’s Pleistocene megafauna. Ecography39: 109–116.
64.
JonesRAWilliamsJWJacksonST (2017) Vegetation history since the last glacial maximum in the Ozark highlands (USA): A new record from Cupola Pond, Missouri. Quaternary Science Reviews170: 174–187.
65.
KahlkeR-D (1999) The History of the Origin, Evolution and Dispersal of the Late Pleistocene Mammuthus-Coelodonta Faunal Complex in Eurasia (Large Mammals). Rapid City: Mammoth Site of Hot Springs.
66.
KamerlingIMSchofieldJEEdwardsKJ, et al. (2017) High-resolution palynology reveals the land use history of a Sami renvall in northern Sweden. Vegetation History and Archaeobotany26: 369–388.
67.
KirbyKJ (2004) A model of a natural wooded landscape in Britain as influenced by large herbivore activity. Forestry77: 405–120.
68.
KirbyKJ (2005) Was the wildwood closed forest or savannah and does it matter for modern nature conservation – Some conclusions. In: HodderKHBullockJMBucklandPV, et al. (eds) Large Herbivores in the Wildwood and Modern Naturalistic Grazing Systems (English Nature Research Reports 648). Peterborough: English Nature, pp. 169–177.
69.
KirbyKJWatkinsC (2015) The forest landscape before farming. In: KirbyKJWatkinsC (eds) Europe’s Changing Woods and Forests, From Wildwood to Managed Landscapes. Wallingford: CAB International, pp. 33–45.
70.
KrugJCBennyGLKellerHW (2004) Coprophilous fungi. In: MuellerGMBillsGFFosterMS (eds) Biodiversity of Fungi, Inventory and Monitoring Methods. San Diego, CA: Elsevier Academic Press, pp. 467–499.
71.
KruysÅWedinM (2009) Phylogenetic relationships and an assessment of traditionally used taxonomic characters in the Sporormiaceae (Pleosporales, Dothideomycetes, Ascomycota), utilising multi-gene phylogenies. Systematics and Biodiversity7: 465–478.
72.
KuthubutheenAJWebsterJ (1986) Effects of water availability on germination, growth and sporulation of coprophilous fungi. Transactions of the British Mycological Society86: 77–91.
73.
LamootICallebautJDegezelleT, et al. (2004) Eliminative behaviour of free-ranging horses: Do they show latrine behaviour or do they defecate where they graze?Applied Animal Behaviour Science86: 105–121.
74.
LancelottiCMadellaM (2012) The ‘invisible’ product: Developing markers for identifying dung in archaeological contexts. Journal of Archaeological Science39: 953–963.
75.
LundqvistN (1972) Nordic Sordariaceae s. lat. Acta Universitas Upsaliensis. Symbolae Botanicae UpsaliensisXX(1).
76.
LütgeBUHatchGPHardyMB (1995) The influence of urine and dung deposition on patch grazing patterns of cattle and sheep in the Southern Tall Grassveld. African Journal of Range and Forage Science12: 104–110.
77.
LydolphMCJacobsenJArctanderP, et al. (2005) Beringian paleoecology inferred from permafrost-preserved fungal DNA. Applied and Environmental Microbiology71: 1012–1017.
78.
MasseeGSalmonES (1902) Researches on coprophilous fungi. II. Annals of Botany16: 57–93.
79.
MitchellFJG (2005) How open were European primeval forests? Hypothesis testing using palaeoecological data. Journal of Ecology93: 168–177.
NewcombeGCampbellJGriffithD, et al. (2016) Revisiting the life cycle of dung fungi, includingSordaria Fimicola. PLoS ONE11: e0147425.
82.
ÖdbergFOFrancis-SmithK (1977) Studies on the formation of ungrazed eliminative areas in fields used by horses. Applied Animal Ethology3: 27–34.
83.
OverpeckJTWebbTPrenticeIC (1985) Quantitative interpretation of fossil pollen spectra: Dissimilarity coefficients and the method of modern analogs. Quaternary Research23: 87–108.
84.
Owen-SmithN (1988) Megaherbivores, the Influence of Very Large Body Size on Ecology (Cambridge Studies in Ecology). Cambridge: Cambridge University Press.
85.
PardoeHSGieseckeTVan der KnaapWO, et al. (2010) Comparing pollen spectra from modified Tauber traps and moss samples: Examples from a selection of woodlands across Europe. Vegetation History and Archaeobotany19: 271–283.
86.
ParkerNEWilliamsJW (2012) Influences of climate, cattle density, and lake morphology on Sporormiella abundances in modern lake sediments in the US Great Plains. The Holocene22: 475–483.
87.
ParviainenJ (2005) Virgin and natural forests in the temperate zone of Europe. Forest Snow and Landscape Research79: 9–18.
88.
PerrottiAGVan AsperenE (2019) Dung fungi as a proxy for megaherbivores: Opportunities and limitations for archaeological applications. Vegetation History and Archaeobotany28: 93–104.
89.
PeterkenGF (1996) Natural Woodland. Cambridge: Cambridge University Press.
90.
PrenticeIC (1985) Pollen representation, source area, and basin size: Toward a unified theory of pollen analysis. Quaternary Research23: 76–86.
91.
ProstKBirkJJLehndorffE, et al. (2017) Steroid biomarkers revisited – Improved source identification of faecal remains in archaeological soil material. PLoS ONE12: e0164882.
92.
RackhamO (2003) Ancient Woodland: Its History, Vegetation and Uses in England. 2nd Edition.Dalbeattie: Castlepoint Press.
93.
RaczkaMFBushMBFolcikAM, et al. (2016) Sporormiella as a tool for detecting the presence of large herbivores in the Neotropics. Biota Neotropica16: e20150090.
94.
RamirezJIJansenPAPoorterL (2018) Effects of wild ungulates on the regeneration, structure and functioning of temperate forests: A semi-quantitative review. Forest Ecology and Management424: 406–419.
95.
RaperDBushM (2009) A test of Sporormiella representation as a predictor of megaherbivore presence and abundance. Quaternary Research71: 490–496.
96.
RichardsonMJ (1972) Coprophilous ascomycetes on different dung types. Transactions of the British Mycological Society58: 37–48.
97.
RichardsonMJ (2001) Diversity and occurrence of coprophilous fungi. Mycological Research105: 387–402.
98.
RuleSBrookBWHaberleSG, et al. (2012) The aftermath of megafaunal extinction: Ecosystem transformation in Pleistocene Australia. Science335: 1483–1486.
99.
SandomCJEjrnæsRHansenMD, et al. (2014) High herbivore density associated with vegetation diversity in interglacial ecosystems. Proceedings of the National Academy of Sciences111: 4162–4167.
100.
SchlützFShumilovskikhL (2017) Non-pollen palynomorphs notes: 1. Type HdV368 (Podospora-type), descriptions of associated species, and the first key to related spore types. Review of Palaeobotany and Palynology239: 47–54.
101.
Shahack-GrossR (2011) Herbivorous livestock dung: Formation, taphonomy, methods for identification, and archaeological significance. Journal of Archaeological Science38: 205–218.
102.
SmithDWhitehouseNBuntingMJ, et al. (2010) Can we characterise ‘openness’ in the Holocene palaeoenvironmental record? Modern analogue studies of insect faunas and pollen spectra from Dunham Massey deer park and Epping Forest, England. The Holocene20: 215–229.
103.
SugitaSGaillardM-JBroströmA (1999) Landscape openness and pollen records: A simulation approach. The Holocene9: 409–421.
104.
SvenningJ-C (2002) A review of natural vegetation openness in north-western Europe. Biological Conservation104: 133–148.
105.
TauberH (1974) A static non-overload pollen collector. New Phytologist73: 359–369.
106.
TrailF (2007) Fungal cannons: Explosive spore discharge in the Ascomycota. FEMS Microbiology Letters276: 12–18.
107.
Van AsperenEN (2017) Fungal diversity on dung of tropical animals in temperate environments: Implications for reconstructing past megafaunal populations. Fungal Ecology28: 25–32.
108.
Van AsperenENKirbyJRHuntCO (2016) The effect of preparation methods on dung fungal spores: Implications for recognition of megafaunal populations. Review of Palaeobotany and Palynology229: 1–8.
109.
Van der KaarsSMillerGHTurneyCSM, et al. (2017) Humans rather than climate the primary cause of Pleistocene megafaunal extinction in Australia. Nature Communications8: 141–142.
110.
VeraFW (2000) Grazing Ecology and Forest History. New York: CABI Publishing.
111.
Von KoenigswaldWHeinrichW-D (1999) Mittelpleistozäne Säugetierfaunen aus Mitteleuropa – der Versuch einer biostratigraphischen Zuordnung. Kaupia – Darmstädter Beiträge zur Naturgeschichte9: 53–112.
112.
WeisbergPJBugmannH (2003) Forest dynamics and ungulate herbivory: From leaf to landscape. Forest Ecology and Management181: 1–12.
113.
WicklowDT (1992) The coprophilous fungal community: An experimental system. In: CarrollGCWicklowDT (eds) The Fungal Community, Its Organization and Role in the Ecosystem. New York: Marcel Dekker, pp. 715–728.
114.
WillisKJBirksHJB (2006) What is natural? The need for a long-term perspective in biodiversity conservation. Science314: 1261–1265.
115.
WilmshurstJMMcGloneMS (2005) Origin of pollen and spores in surface lake sediments: Comparison of modern palynomorph assemblages in moss cushions, surface soils and surface lake sediments. Review of Palaeobotany and Palynology136: 1–15.
116.
WoodJRWilmshurstJM (2012) Wetland soil moisture complicates the use ofSporormiella to trace past herbivore populations. Journal of Quaternary Science27: 254–259.
117.
WoodJRWilmshurstJM (2013) Accumulation rates or percentages? How to quantify Sporormiella and other coprophilous fungal spores to detect late Quaternary megafaunal extinction events. Quaternary Science Reviews77: 1–3.
118.
WrightHEJrMcAndrewsJHVan ZeistW (1967) Modern pollen rain in western Iran, and its relation to plant geography and Quaternary vegetation history. Journal of Ecology55: 415–443.
119.
YafettoLCarrollLCuiY, et al. (2008) The fastest flights in nature: High-speed spore discharge mechanisms among fungi. PLoS ONE3: e3237.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
