Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-18T18:52:18.721Z Has data issue: false hasContentIssue false
  • English
  • Français

A multidisciplinary study of a Late Pleistocene arctic ground squirrel (Urocitellus parryii) midden from Yukon, Canada

Published online by Cambridge University Press:  20 November 2017

Bram W. Langeveld ,
Dick Mol ,
Grant D. Zazula ,
Barbara Gravendeel ,
Marcel Eurlings ,
Crystal N.H. McMichael ,
Dick Groenenberg ,
Guido B.A. van Reenen ,
Mona Palmeira  and
Johnny Vogel
...Show all authors
Bram W. Langeveld*
Affiliation:
Natural History Museum Rotterdam, Westzeedijk 345, 3015 AA Rotterdam, The Netherlands
Dick Mol
Affiliation:
Natural History Museum Rotterdam, Westzeedijk 345, 3015 AA Rotterdam, The Netherlands
Grant D. Zazula
Affiliation:
Yukon Palaeontology Program, Yukon Government, P.O. Box 2703, Whitehorse, Yukon, Y1A 0M5, Canada
Barbara Gravendeel
Affiliation:
Endless Forms group, Naturalis Biodiversity Center, Sylviusweg 72, 2333 BE Leiden, The Netherlands
Marcel Eurlings
Affiliation:
Laboratories of Naturalis Biodiversity Center, Sylviusweg 72, 2333 BE Leiden, The Netherlands
Crystal N.H. McMichael
Affiliation:
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, The Netherlands
Dick Groenenberg
Affiliation:
Endless Forms group, Naturalis Biodiversity Center, Sylviusweg 72, 2333 BE Leiden, The Netherlands
Guido B.A. van Reenen
Affiliation:
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, The Netherlands
Mona Palmeira
Affiliation:
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, The Netherlands
Johnny Vogel
Affiliation:
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, The Netherlands
Bas van Geel
Affiliation:
Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, The Netherlands
*
*Corresponding author at: Natural History Museum Rotterdam, Westzeedijk 345, 3015 AA Rotterdam, The Netherlands. E-mail address: langeveld@hetnatuurhistorisch.nl (B.W. Langeveld).
Get access Rights & Permissions [Opens in a new window]

Abstract

Middens (nests and caches) of Late Pleistocene arctic ground squirrels (Urocitellus parryii) that are preserved in the permafrost of Beringia archive valuable paleoecological data. Arctic ground squirrels selectively include the plant material placed in middens. To account for this selectivity bias, we used a multi-proxy approach that includes ancient DNA (aDNA) and macro- and microfossil analyses. Here, we provide insight into Pleistocene vegetation conditions using macrofossils, pollen, phytoliths and non-pollen palynomorphs, and aDNA collected from one such midden from the Yukon Territory (Canada), which was formed between 30,740 and 30,380 cal yr BP. aDNA confirmed the midden was constructed by U. parryii. We recovered 39 vascular plant and bryophyte genera and 68 fungal genera from the midden samples. Grass and other herbaceous families dominated vegetation assemblages according to all proxies. aDNA data yielded several records of vascular plants that are outside their current biogeographic range, while some of the recovered fungi yielded additional evidence for local occurrence of Picea trees during glacial conditions. We propose that future work on fossil middens should combine the study of macro- and microfossils with aDNA analysis to get the most out of these environmental archives.

Keywords

Ancient DNAGround squirrelPaleoecologyWisconsinanYukon
Type
Research Article
Information
Quaternary Research , Volume 89 , Issue 1: Tribute to Daniel Livingstone and Paul Colinvaux , January 2018 , pp. 333 - 351
Copyright
Copyright © University of Washington. Published by Cambridge University Press, 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., 1990. Basic local alignment search tool. Journal of Molecular Biology 215, 403410.CrossRefGoogle ScholarPubMed
Ames, L.M., 1961. A monograph of the Chaetomiaceae. The United States Army Research and Development Series 2, 1–125.Google Scholar
Anderson, R.S., Homola, R.L., Davis, R.B., Jacobson, G.L. Jr., 1984. Fossil remains of the mycorrhizal fungal Glomus fasciculatum complex in postglacial lake sediments from Maine. Canadian Journal of Botany 62, 2325–2328.Google Scholar
Beug, H., 2004. Leitfaden der Pollenbestimmung für Mitteleuropa und angrenzende Gebiete. Verlag Dr. Friedrich Pfeil, München.Google Scholar
Birks, H.H., 2007. Plant Macrofossil Introduction. In: Elias, S.A. (Ed.), Encyclopedia of Quaternary Science. Elsevier, Amsterdam, pp. 2266–2288.Google Scholar
Blankenberg, D., von Kuster, G., Coraor, N., Ananda, G., Lazarus, R., Mangan, M., Nekrutenko, A., Taylor, J., 2010. Galaxy: a web-based genome analysis tool for experimentalists. Current Protocols in Molecular Biology Jan, Chapter 19: Unit 19.10.1–21. http://dx.doi.org/ 10.1002/0471142727.mb1910s89.Google Scholar
Blinnikov, M.S., Gaglioti, B.V., Walker, D.A., Wooller, M.J., Zazula, G.D., 2011. Pleistocene graminoid-dominated ecosystems in the Arctic. Quaternary Science Reviews 30, 2906–2929.Google Scholar
Brubaker, L.B., Anderson, P.M., Edwards, M.E., Lozhkin, A.V., 2005. Beringia as a glacial refugium for boreal trees and shrubs: new perspectives from mapped pollen data. Journal of Biogeography 32, 833–848.Google Scholar
Buck, C.L., Barnes, B.M., 1999. Annual cycle of body condition and hibernation in free-living arctic ground squirrels. Journal of Mammalogy 80, 430–442.Google Scholar
Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., Madden, T.L., 2009. BLAST+architecture and applications. BMC Bioinformatics 10, 421.Google Scholar
Cappers, R.T.J., Bekker, R.M., Jans, J.E.A., 2006. Digitale Zadenatlas van Nederland/Digital Seed Atlas of the Netherlands. Groningen Archaeological Studies 4. Barkhuis Publishing and Groningen University Library, Groningen.Google Scholar
Cavalier-Smith, T., 1981. Eukaryote kingdoms: seven or nine? Biosystems 14, 461–481.Google Scholar
Chambers, F.M., van Geel, B., van der Linden, M., 2011. Considerations for the preparation of peat samples for palynology, and for the counting of pollen and non-pollen palynomorphs. Mires and Peat 7, 1–14.Google Scholar
Cody, W.J., 2000. Flora of the Yukon Territory. National Research Council (NRC) Press, Ottawa, Canada.Google Scholar
Cooper, A., Poinar, H.N., 2000. Ancient DNA: do it right or not at all. Science 289, 1139.Google Scholar
Crum, H.A., Anderson, L.E., 1981. Mosses of Eastern North America. Vol. 1 and 2. Columbia University Press, New York.Google Scholar
Dahlstrom, J.L., Smith, J.E., Weber, N.S., 2000. Mycorrhiza-like interaction by Morchella with species of the Pinaceae in pure culture synthesis. Mycorrhiza 9, 279–285.Google Scholar
Davis, M.B., 1963. On the theory of pollen analysis. American Journal of Science 261, 897–912.CrossRefGoogle Scholar
Davis, O.K., 1987. Spores of the dung fungus Sporormiella: increased abundance in historic sediments and before Pleistocene megafaunal extinction. Quaternary Research 28, 290–294.Google Scholar
Edwards, M.E., Armbruster, W.S., 1989. A tundra-steppe transition on Kathul Mountain, Alaska, USA. Arctic and Alpine research 21, 296–304.CrossRefGoogle Scholar
Elias, S.A., Brigham-Grette, J., 2007. Late Pleistocene Events in Beringia. In: Elias, S.A. (Ed.), Encyclopedia of Quaternary Science. Elsevier, Amsterdam, pp. 1057–1066.Google Scholar
Elias, S.A., 2010. 15 Ancient DNA Studies. Developments in Quaternary Sciences 12, 223–228.Google Scholar
Flora of North America, 2016. Flora of North America Database (accessed April 6, 2016) http://www.efloras.org/flora_page.aspx?flora_id=1.Google Scholar
Froese, D.G., Zazula, G.D., Reyes, A.V., 2006. Seasonality of the late Pleistocene Dawson tephra and exceptional preservation of a buried riparian surface in central Yukon Territory, Canada. Quaternary Science Reviews 25, 1542–1551.Google Scholar
Gaglioti, B.V., Barnes, B.M., Zazula, G.D., Beaudoin, A.B., Wooller, M.J., 2011. Late Pleistocene paleoecology of arctic ground squirrel (Urocitellus parryii) caches and nests from interior Alaska’s mammoth steppe ecosystem, USA. Quaternary Research 76, 373–382.Google Scholar
Geml, J., Laursen, G.A., O’Neill, K., Nusbaum, H.C., Taylor, D.L., 2006. Beringian origins and cryptic speciation events in the fly agaric (Amanita muscaria). Molecular Ecology 15, 225–239.CrossRefGoogle ScholarPubMed
Geml, J., Kauff, F., Laursen, G.A., Taylor, D.L., 2010. Genetic studies point to Beringia as a biodiversity hotspot for high-latitude fungi. Alaska Park Science 8, 37–41.Google Scholar
Giardine, B., Riemer, C., Hardison, R.C., Burhans, R., Elnitski, L., Shah, P., Zhang, Y., et al., 2005. Galaxy: a platform for interactive large-scale genome analysis. Genome Research 15, 1451–1455.Google Scholar
Gill, J.L., McLauchlan, K.K., Skibbe, A.M., Goring, S., Zirbel, C.R., Williams, J.W., 2013. Linking abundances of the dung fungus Sporormiella to the density of bison: implications for assessing grazing by megaherbivores in palaeorecords. Journal of Ecology 101, 1125–1136.Google Scholar
Goecks, J., Nekrutenko, A., Taylor, J., The Galaxy Team, 2010. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biology 11, R86. http://dx.doi.org/10.1186/gb-2010-11-8-r86.Google Scholar
Gravendeel, B., Protopopov, A., Bull, I., Duijm, E., Gill, F., Nieman, A., Rudaya, N., et al. 2014. Multiproxy study of the last meal of a mid-Holocene Oyogos Yar horse, Sakha Republic, Russia. The Holocene 24, 1288–1296.Google Scholar
Guthrie, R.D., 1990. Frozen Fauna of the Mammoth Steppe: The Story of Blue Babe. The University of Chicago Press, Chicago.Google Scholar
Harington, C.R., 2011. Pleistocene vertebrates of the Yukon Territory. Quaternary Science Reviews 30, 2341–2354.CrossRefGoogle Scholar
Hasebe, M., Omori, T., Nakazawa, M., Sano, T., Kato, M., Iwatsuki, K., 1994. rbcL gene sequences provide evidence for the evolutionary lineages of leptosporangiate ferns. Proceedings of the National Academy of Sciences of the United States of America 91, 5730–5734.Google Scholar
Hofreiter, M., Poinar, H.N., Spaulding, W.G., Bauer, K., Martin, P.S., Possnert, G., Pääbo, S., 2000. A molecular analysis of ground sloth diet through the last glaciation. Molecular Ecology 9, 1975–1984.Google Scholar
Jacobson, G.L., Bradshaw, R.H.W., 1981. The selection of sites for paleovegetational studies. Quaternary Research 16, 80–96.Google Scholar
Juggins, S., 2003. C2 Program Version 1.4. Department of Geography, University of Newcastle, Newcastle upon Tyne, UK (accessed 4 June 2017). http://www.campus.ncl.ac.uk/staff/Stephen.Juggins/software/c2home.htm.Google Scholar
Kapp, R.O., Davis, O.K., King, J.E., 2000. Ronald O. Kapp’s Pollen and Spores. 2nd ed. The American Association of Stratigraphic Palynologists Foundation, College Station, Texas, USA.Google Scholar
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., et al., 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.Google Scholar
Kołaczek, P., Zubek, S., Błaszkowski, J., Mleczko, P., Margielewski, W., 2013. Erosion or plant succession — How to interpret the presence of arbuscular mycorrhizal fungi (Glomeromycota) spores in pollen profiles collected from mires. Review of Palaeobotany and Palynology 189, 29–37.Google Scholar
Lawton, E., 1971. Moss Flora of the Pacific Northwest. The Hattori Botanical Laboratory, Nichinan, Japan.Google Scholar
Lydolph, M.C., Jacobsen, J., Arctander, P., Gilbert, M.T.P., Gilichinsky, D.A., Hansen, A.J., Willerslev, E., Lange, L., 2005. Beringian paleoecology inferred from permafrost-preserved fungal DNA. Applied and Environmental Microbiology 71, 1012–1017.Google Scholar
Mann, D.H., Peteet, D.M., Reanier, R.E., Kunz, M.L., 2002. Responses of an arctic landscape to Lateglacial and early Holocene climatic changes: the importance of moisture. Quaternary Science Reviews 21, 997–1021.Google Scholar
Matthews, J.V., 1982. East Beringia during Late Wisconsin time: a review of the biotic evidence. In: Hopkins, D.M., Matthews, J.V., Schweger C.E., Young, S.B. (Eds.), Paleoecology of Beringia. Elsevier, Amsterdam, pp. 127–150.Google Scholar
Mauquoy, D., van Geel, B., 2007. Mire and peat macros. In: Elias, S.A. (Ed.), Encyclopedia of Quaternary Science, Elsevier, Amsterdam, pp. 2315–2336.Google Scholar
Mauquoy, D., Hughes, P.D.M., van Geel, B., 2011. A protocol for plant macrofossil analysis of peat deposits. Mires and Peat 7, Article 6, 1–5.Google Scholar
McAndrews, J.H., Berti, A.A., Norris, G., 1973. Key to the Quaternary pollen and spores of the Great Lakes region. Life Sciences Miscellaneous Publication, Royal Ontario Museum. The University of Toronto Press, Toronto.Google Scholar
Miola, A., 2012. Tools for Non-Pollen Palynomorphs (NPPs) analysis: a list of Quaternary NPP types and reference literature in English language (1972–2011). Review of Palaeobotany and Palynology 186, 142–161.Google Scholar
Montoya, E., Rull, V., van Geel, B., 2010. Non-pollen palynomorphs from surface sediments along an altitudinal transect of the Venezuelan Andes. Palaeogeography, Palaeoclimatology, Palaeoecology 297, 169–183.Google Scholar
Morcote-Ríos, G., Giraldo-Cañas, D., Raz, L., 2015. Catálogo ilustrado de fitolitos contemporáneos con énfasis arqueológico y paleoecológico I. Gramíneas amazónicas de Colombia. Universidad Nacional de Colombia, Bogotá, Colombia.Google Scholar
Piperno, D.R., 2006. Phytoliths: a comprehensive guide for archaeologists and paleoecologists. Alta Mira Press, Lanham, Maryland.Google Scholar
Pirozynski, K.A., Carter, A., Day, R.G., 1984. Fungal remains in Pleistocene ground squirrel dung from Yukon Territory, Canada. Quaternary Research 22, 375–382.Google Scholar
R Development Core Team, 2011. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Reimer, P.J., Bard, E., Bayliss, A., Beck, J.W., Blackwell, P.G., Bronk, C.B., Buck, C.E., et al., 2013. IntCal13 and marine13 radiocarbon age calibration curves 0–50,000 years cal BP. Radiocarbon 55, 1869–1887.Google Scholar
Richardson, M.J., Watling, R., 1997. Keys to Fungi on Dung. British Mycological Society, Stourbridge.Google Scholar
Rohland, N., Hofreiter, M., 2007. Ancient DNA extraction from bones and teeth. Nature Protocols 2, 1756–1762.CrossRefGoogle ScholarPubMed
Schoch, C.L., Seifert, K.B., Huhndorf, S., Robert, V., Spougea, J.L., Levesque, C.A., Chen, W., Fungal Barcoding Consortium, 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences of the United States of America 109, 6241–6246.CrossRefGoogle ScholarPubMed
Soreng, R.J., Gillespie, L.J., Koba, H., Boudko, E., Bull, R.D., 2015. Molecular and morphological evidence for a new grass genus, Dupontiopsis (Poaceae tribe Poeae subtribe Poinae s.l.), endemic to alpine Japan, and implications for the reticulate origin of Dupontia and Arctophila within Poinae s.l. Journal of Systematics and Evolution 53, 138–162.Google Scholar
Stalpers, J.A., 1993. The Aphyllophoraceous fungi I: keys to the species of the Thelephorales. Studies in Mycology 35, 1–168.Google Scholar
Taberlet, P., Coissac, E., Pompanon, F., Gielly, L., Miquel, C., Valentini, A., Vermat, T., Corthier, G., Brochmann, C., Willerslev, E., 2007. Power and limitations of the chloroplast trnL (UAA) intron for plant DNA barcoding. Nucleic Acids Research 35, 1–8.Google Scholar
The Plant List, 2013. Version 1.1 (accessed March 14, 2016). http://www.theplantlist.org.Google Scholar
van Geel, B., 1978. A palaeoecological study of Holocene peat bog sections in Germany and the Netherlands based on the analysis of pollen, spores and macro- and microscopic remains of fungi, algae, cormophytes and animals. Review of Palaeobotany and Palynology 25, 1–120.Google Scholar
van Geel, B., Aptroot, A., 2006. Fossil ascomycetes in Quaternary deposits. Nova Hedwigia 82, 313–329.CrossRefGoogle Scholar
van Geel, B., Aptroot, A., Baittinger, C., Birks, H.H., Bull, I.D., Cross, H.B., Evershed, R.P., et al., 2008. The ecological implications of a Yakutian mammoth’s last meal. Quaternary Research 69, 361–376.Google Scholar
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. Journal of Archaeological Science 30, 873–883.CrossRefGoogle Scholar
van Geel, B., Fisher, D.C., Rountrey, A.N., van Arkel, J., Duivenvoorden, J.F., Nieman, A.M., van Reenen, G.B.A., Tikhonov, A.N., Buigues, B., Gravendeel, B., 2011b. Palaeo-environmental and dietary analysis of intestinal contents of a mammoth calf (Yamal Peninsula, northwest Siberia). Quaternary Science Reviews 30, 3935–3946.Google Scholar
van Geel, B., Guthrie, R.D., Altmann, J.G., Broekens, P., Bull, I.D., Gill, F.L., Jansen, B., Nieman, A.M., Gravendeel, B., 2011a. Mycological evidence of coprophagy from the feces of an Alaskan Late Glacial mammoth. Quaternary Science Reviews 30, 2289–2303.Google Scholar
van Geel, B., Zazula, G.D., Schweger, C.E., 2007. Spores of coprophilous fungi from under the Dawson tephra (25,300 14C years BP), Yukon Territory, northwestern Canada. Palaeogeography, Palaeoclimatology, Palaeoecology 252, 481–485.Google Scholar
VASCAN. 2016. Database of Vascular Plants of Canada (accessed 7 April 2016) http://data.canadensys.net/vascan/search.Google Scholar
Vilgalys lab, 2015. Internal Transcribed Spacer (ITS) Region Primers (accessed 23 October 2015). http://sites.biology.duke.edu/fungi/mycolab/primers.htm#Internal%20transcribed%20spacer%20%28ITS%29%20region%20primers.Google Scholar
Vitt, D.H, Buck, W.R., 2001. Bryophyte Flora of North America (accessed March 14, 2016). http://www.mobot.org/plantscience/BFNA/bfnamenu.htm.Google Scholar
Westgate, J.A., Preece, S.J., Kotler, E., Hall, S., 2000. Dawson tephra: a prominent stratigraphic marker of Late Wisconsinan age in west-central Yukon, Canada. Canadian Journal of Earth Sciences 37, 621–627.Google Scholar
White, T.J., Bruns, T., Lee, S., Taylor, J., 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis, M.A., Gelfand, D.H., Sninsky, J.J. (Eds.), PCR Protocols: A Guide to Methods and Applications. Academic Press, San Diego, pp. 315–322.Google Scholar
Willerslev, E. et al., 2014. Fifty thousand years of Arctic vegetation and megafaunal diet. Nature 506, 47–51.Google Scholar
Wooller, M.J., Zazula, G.D., Blinnikov, M., Gaglioti, B.V., Bigelow, N.H., Sandorn, P., Kuzmina, S., La Farge, C., 2011. The detailed palaeoecology of a mid-Wisconsinan interstadial (ca. 32 000 14C a BP) vegetation surface from interior Alaska. Journal of Quaternary Science 26, 746–756.Google Scholar
Zazula, G.D., Froese, D.G., Elias, S.A., Kuzmina, S., La Farge, C., Reyes, A.V., Sanborn, P.T., Schweger, C.E., Smith, C.A.S., Mathewes, R.W., 2006b. Vegetation buried under Dawson tephra (25,300 14C years BP) and locally diverse late Pleistocene paleoenvironments of Goldbottom Creek, Yukon, Canada. Palaeogeography, Palaeoclimatology, Palaeoecology 242, 253–286.Google Scholar
Zazula, G.D., Froese, D.G., Elias, S.A., Kuzmina, S., Mathewes, R.W., 2007. Arctic ground squirrels of the mammoth-steppe: paleoecology of middens from the last glaciation, Yukon Territory, Canada. Quaternary Science Reviews 26, 979–1003.Google Scholar
Zazula, G.D., Froese, D.G., Elias, S.A., Kuzmina, S., Mathewes, R.W., 2011. Early Wisconsinan (MIS 4) Arctic ground squirrel middens and a squirrel-eye-view of the mammoth-steppe. Quaternary Science Reviews 30, 2220–2237.Google Scholar
Zazula, G.D., Froese, D.G., Westgate, J.A., La Farge, C., Mathewes, R.W., 2005. Paleoecology of Beringian “packrat” middens from central Yukon Territory. Quaternary Research 63, 189–198.Google Scholar
Zazula, G.D., Mathewes, R.W., Harestad, A.S., 2006a. Cache Selection by Arctic Ground Squirrels Inhabiting Boreal-steppe Meadows of Southwest Yukon Territory, Canada. Arctic, Antarctic, and Alpine Research 38, 631–638.Google Scholar
Zazula, G.D., Schweger, C.E., Beaudoin, A.B., McCourt, G.H., 2006c. Macrofossil and pollen evidence for full-glacial steppe within an ecological mosaic along the Bluefish River, eastern Beringia. Quaternary International 142–143, 2–19.Google Scholar
Zazula, G.D., Telka, A.M., Harington, C.R., Schweger, C.E., Mathewes, R.W., 2006d. New spruce (Picea spp.) macrofossils from Yukon Territory: implications for Late Pleistocene refugia in Eastern Beringia. Arctic 59, 391–400.Google Scholar
Zimov, S.A., Zimov, N.S., Chapin, F.S. III, 2012. Chapter 10: The past and future of the Mammoth Steppe Ecosystem. In: Louys, J. (Ed.), Paleontology in Ecology and Conservation. Springer Earth System Sciences, Springer-Verlag Berlin Heidelberg, pp. 193–225.Google Scholar
Supplementary material: File

Langeveld et al supplementary material

Langeveld et al supplementary material 1

Download Langeveld et al supplementary material(File)
File 40.4 MB
Supplementary material: File

Langeveld et al supplementary material

Langeveld et al supplementary material 2

Download Langeveld et al supplementary material(File)
File 34.6 MB
Supplementary material: File

Langeveld et al supplementary material

Langeveld et al supplementary material 3

Download Langeveld et al supplementary material(File)
File 66.8 MB
Supplementary material: File

Langeveld et al supplementary material

Langeveld et al supplementary material 4

Download Langeveld et al supplementary material(File)
File 40.4 MB
Supplementary material: File

Langeveld et al supplementary material

Langeveld et al supplementary material 5

Download Langeveld et al supplementary material(File)
File 16.3 MB
Supplementary material: File

Langeveld et al supplementary material

Langeveld et al supplementary material 6

Download Langeveld et al supplementary material(File)
File 6.5 MB