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Research Article

White bark in birch species as a warning signal for bark-stripping mammals

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Pages 93-109 | Received 03 Jul 2022, Accepted 06 Sep 2022, Published online: 07 Oct 2022

References

  • Agrawal A. 2007. Macroevolution of plant defense strategies. Trends Ecol Evol. 22(2):103–109. doi:10.1016/j.tree.2006.10.012.
  • Alakurtti S, Mäkelä T, Koskimies S, Yli-Kauhaluoma JT. 2006. Pharmacological properties of the ubiquitous natural product betulin. Eur J Pharm Sci. 29(1):1–13. doi:10.1016/j.ejps.2006.04.006.
  • Alonso-Serra J, Safronov O, Lim KJ, Fraser-Miller SJ, Blokhina OB, Campilho A, Chong SL, Fagerstedt K, Haavikko R, Helariutta Y, et al. 2019. Tissue-Specific study across the stem reveals the chemistry and transcriptome dynamics of birch bark. New Phytol. 222:1816–1831. doi:10.1111/nph.15725.
  • Atkinson AMD. 1992. Betula Pendula Roth (B. Verrucosa Ehrh.) and B. Pubescens Ehrh. J Ecol. 80:837–870.
  • Baker WL, Munroe JA, Hessl AE. 1997. The effects of elk on aspen in the winter range in Rocky Mountain National Park. Ecography (Cop). 20(2):155–165. doi:https://doi.org/10.1111/j.1600-0587.1997.tb00358.x.
  • Baraniewicz M, Perzanowski K. 2015. Are reintroduced Wisents a threat to mountain forests? Ann Zool Fennici. 52(5–6):301–312. doi:https://doi.org/10.5735/086.052.0505.
  • Bennett RN, Wallsgrove RM. 1994. Secondary metabolites in plant defence mechanisms. New Phytol. 127(4):617–633. doi:https://doi.org/10.1111/j.1469-8137.1994.tb02968.x.
  • Bergman M, Iason GR, Hester AJ. 2005. Feeding patterns by roe deer and rabbits on pine, willow and birch in relation to spatial arrangement. Oikos. 109(3):513–520. doi:https://doi.org/10.1111/j.0030-1299.2005.13794.x.
  • Bergvall UA, Co M, Bergström R, Sjöberg PJR, Waldebäck M, Turner C. 2013. Anti-Browsing effects of birch bark extract on fallow deer. Eur J for Res. 132:717–725. doi:10.1007/s10342-013-0709-y.
  • Bina H, Yousefzadeh H, Ali SS, Esmailpour M. 2016. Phylogenetic relationships, molecular taxonomy, biogeography of Betula, with emphasis on phylogenetic position of Iranian populations. Tree Genet Genomes. 12(5):1–17. doi:10.1007/s11295-016-1037-4.
  • Borowski S, Kossak S. 1972. The natural food preferences of the European bison in seasons free of snow cover. Acta Theriol (Warsz). 17:151–169. doi:10.4098/at.arch.72-13.
  • Bryant JP, Julkunen-Tiitto R. 1995. Ontogenic development of chemical defense by seedling Resin Birch: energy cost of defense production. J Chem Ecol. 21(7):883–896. doi:10.1007/BF02033796.
  • Bryant JP, Provenza FD, Pastor J, Reichardt PB, Clausen TP, du Toit JT. 1991. Interactions between woody plants and browsing mammals mediated by secondary metabolites. Annu Rev Ecol Syst. 22:431–446. doi:10.1146/annurev.es.22.110191.002243.
  • Campbell SA, Borden JH. 2005. Bark reflectance spectra of conifers and angiosperms: implications for host discrimination by coniferophagous bark and timber beetles. Can Entomol. 137(6):719–722. doi:https://doi.org/10.4039/N04-082.
  • Caro T, Ruxton G. 2019. Aposematism: unpacking the defences. Trends Ecol Evol. 34(7):595–604. doi:https://doi.org/10.1016/j.tree.2019.02.015.
  • Chen CC, Crilly N 2014. Modularity, redundancy and degeneracy: cross-domain perspectives on key design principles. 8th Annual IEEE International Systems Conference, SysCon 2014 - Proceedings; Ottawa, Canada, p. 546–553.
  • Chen Z, Manchester S, Sun H. 1999. Phylogeny and evolution of the Betulaceae as inferred from DNA sequences, morphology and paleobotany. Am J Bot. 86(8):1168–1181. doi:10.2307/2656981.
  • Clauss M, Frey R, Kiefer B, Lechner-Doll M, Loehlein W, Polster C, Rössner GE, Streich WJ. 2003. The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters. Oecologia. 136:14–27. doi:10.1007/s00442-003-1254-z.
  • Curtis JD. 1944. Appraisal of porcupine damage. J Wildl Manage. 8(1):88–91. doi:10.2307/3796204.
  • D’Angelo GJ, Glasser A, Wendt M, Williams GA, Osborn DA, Gallagher GR, Warren RJ, Miller KV, Pardue MT. 2008. Visual specialization of an herbivore prey species, the white-tailed deer. Can J Zool. 86(7):735–743. doi:https://doi.org/10.1139/Z08-050.
  • Demment MW, Van Soest PJ. 1985. A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am Nat. 125(5):641–672. doi:https://doi.org/10.1086/284369.
  • Fehér Á, Szemethy L, Katona K. 2016. Selective debarking by ungulates in temperate deciduous forests: preference towards tree species and stem girth. Eur J for Res. 135(6):1131–1143. doi:https://doi.org/10.1007/s10342-016-1000-9.
  • Fischer A, Lindner M, Abs C, Lasch P. 2002. Vegetation dynamics in central european forest ecosystems (near-natural as well as managed) after storm events. Folia Geobot. 37(1):17–32. doi:https://doi.org/10.1007/BF02803188.
  • Freeland WJ, Janzen DH. 1974. Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat. 108(961):269–289. doi:https://doi.org/10.1086/282907.
  • Fryxell JM, Doucet CM. 1993. Diet choice and the functional response of beavers. Ecology. 74(5):1297–1306. doi:https://doi.org/10.2307/1940060.
  • Gacic D, Danilovic M, Zubic G, Cirovic P. 2012. Bark stripping damage by red deer (Cervus elaphus L.) in the fenced rearing centre “Lomnicka Reka“. Glas Sumar Fak/bull Fac for. 105:35–50. doi:10.2298/gsf1205035g.
  • Gerhardt P, Arnold JM, Hackländer K, Hochbichler E. 2013. Determinants of deer impact in European forests - a systematic literature analysis. For Ecol Manage. 310:173–186. doi:10.1016/j.foreco.2013.08.030.
  • Gill RMA. 1992a. A review of damage by mammals in North temperate forests. 3. Deer. Forestry. 65:145–169. doi:10.1093/forestry/65.2.145.
  • Gill RMA. 1992b. A review of damage by mammals in north temperate forests. 2. Small mammals. Forestry. 65(3):281–308. doi:https://doi.org/10.1093/forestry/65.3.281.
  • Guilford T, Dawkins MS. 1991. Receiver psychology and the evolution of animal signals. Anim Behav. 42(1):1–14. doi:https://doi.org/10.1016/S0003-3472(05)80600-1.
  • Hahn C, Vospernik S. 2022. Position, size, and spatial patterns of bark stripping wounds inflicted by red deer (Cervus elavus L.) on Norway spruce using generalized additive models in Austria. Ann for Sci. 79(1):1–16. doi:https://doi.org/10.1186/s13595-022-01134-y.
  • Harju A. 1996. Effect of birch (Betula pendula) bark and food protein level on root voles (Microtus oeconomus): I. Food consumption, growth and mortality. J Chem Ecol. 22(4):719–728. doi:https://doi.org/10.1007/BF02033581.
  • Harrington LA, Feber R, Raynor R, Macdonald DW 2015. SNH commissioned report 685: The Scottish Beaver trial: ecological monitoring of the European beaver Castor fiber and other riparian mammals 2009-2014, final report.
  • Haynes G. 2012. Elephants (and extinct relatives) as earth-movers and ecosystem engineers. Geomorphology. 157–158:99–107. doi:10.1016/j.geomorph.2011.04.045.
  • Hebets EA, Barron AB, Balakrishnan CN, Hauber ME, Mason PH, Hoke KL. 2016. A systems approach to animal communication. Proc R Soc B Biol Sci. 283(1826):20152889. doi:10.1098/rspb.2015.2889.
  • Henker K 2009. What do beaver eat? [accessed 2022 August 25]. https://www.grandcanyontrust.org/sites/default/files/ut_beaverDietReview.pdf
  • Hummel J, Südekum KH, Streich WJ, Clauss M. 2006. Forage fermentation patterns and their implications for herbivore ingesta retention times. Funct Ecol. 20(6):989–1002. doi:https://doi.org/10.1111/j.1365-2435.2006.01206.x.
  • Hynynen J, Niemistö P, Viherä-Aarnio A, Brunner A, Hein S, Velling P. 2010. Silviculture of birch (Betula pendula Roth and Betula pubescens Ehrh.) in Northern Europe. Forestry. 83(1):103–119. doi:https://doi.org/10.1093/forestry/cpp035.
  • Iason G. 2005. The role of plant secondary metabolites in mammalian herbivory: ecological perspectives. Proc Nutr Soc. 64(1):123–131. doi:https://doi.org/10.1079/pns2004415.
  • Jacobs GH. 1993. The distribution and nature of colour vision among the mammals. Biol Rev Camb Philos Soc. 68(3):413. doi:https://doi.org/10.1111/j.1469-185x.1993.tb00738.x.
  • Jamrozy G. 1980. Winter food resources and food preferences of red deer in Carpathian forests. Acta Theriol (Warsz). 25:221–238. doi:10.4098/at.arch.80-17.
  • Johnston CA, Johnston CA. 2017. Beaver Loggers: beaver herbivory alters forest structure. In: Beavers: boreal ecosystem engineers. New York (NY): Springer; pp. 91–116.
  • Karels TJ, Boonstra R. 2003. Reducing solar heat gain during winter: the role of white bark in northern deciduous trees. Arctic. 56(2):168–174. doi:10.14430/arctic612.
  • Kavanagh PH, Shaw RC, Burns KC. 2016. Potential aposematism in an insular tree species: are signals dishonest early in ontogeny? Biol J Linn Soc. 118(4):951–958. doi:https://doi.org/10.1111/bij.12785.
  • Kiffner C, Rößiger E, Trisl O, Schulz R, Rühe F. 2008. Probability of recent bark stripping damage by red deer (Cervus elaphus) on Norway spruce (Picea abies) in a low mountain range in Germany – a preliminary analysis. Silva Fenn. 42(1):125–134. doi:10.14214/sf.269.
  • Kinnaird JW, Welch D, Cummins C. 1979. Selective stripping of rowan (Sorbus aucuparia L.) bark by cattle in North-east Scotland. Trans Bot Soc Edinburgh. 43(2):115–125. doi:https://doi.org/10.1080/03746607908685344.
  • Klich D. 2017. Selective bark stripping of various tree species by Polish horses in relation to bark detachability. For Ecol Manage. 384:65–71. doi:10.1016/j.foreco.2016.10.019.
  • Krasutsky PA. 2006. Birch bark research and development. Nat Prod Rep. 23(6):919. doi:https://doi.org/10.1039/b606816b.
  • Kuiters AT, Van Der Sluijs LAM, Wytema GA. 2006. Selective bark-stripping of beech, Fagus sylvatica, by free-ranging horses. For Ecol Manage. 222:1–8. doi:10.1016/j.foreco.2005.09.019.
  • Laitinen M-L, Julkunen-Tiitto R, Tahvanainen J, Heinonen J, Rousi M. 2005. Variation in birch(Betula Pendula) shoot secondary chemistry due to genotype, environment and ontogeny. J Chem Ecol. 31(4):697–717. doi:10.1007/s10886-005-3539-7.
  • Lambert WD. 1992. The feeding habits of the shovel-tusked gomphotheres: evidence from tusk wear patterns. Paleobiology. 18:132–147. doi:10.1017/S0094837300013932.
  • Lawes MJ, Midgley JJ, Clarke PJ, Jones R. 2013. Costs and benefits of relative bark thickness in relation to fire damage: a savanna/forest contrast. J Ecol. 101(2):517–524. doi:https://doi.org/10.1111/1365-2745.12035.
  • Lev-Yadun S. 2001. Aposematic (warning) coloration associated with thorns in higher plants. J Theor Biol. 210(3):385–388. doi:https://doi.org/10.1006/jtbi.2001.2315.
  • Lev-Yadun S. 2014. Why is latex usually white and only sometimes yellow, orange or red? Simultaneous visual and chemical plant defense. Chemoecology. 24(5):215–218. doi:https://doi.org/10.1007/s00049-014-0160-7.
  • Lev-Yadun S. 2016. Defensive (anti-herbivory) coloration in land plants. New York (NY): Springer.
  • Lev-Yadun S. 2019. Why is the bark of common temperate betula and populus species white? Int J Plant Sci. 180:632–642. doi:10.1086/702760.
  • Ludt CJ, Schroeder W, Rottmann O, Kuehn R. 2004. Mitochondrial DNA phylogeography of red deer (Cervus elaphus). Mol Phylogenet Evol. 31(3):1064–1083. doi:https://doi.org/10.1016/j.ympev.2003.10.003.
  • Lutz H. 1956. Damage to paper birch by red squirrels in Alaska. J For. 54:31–33.
  • Mackie RI. 2002. Mutualistic fermentative digestion in the gastrointestinal tract: diversity and evolution. Integr Comp Biol. 42(2):319–326. doi:https://doi.org/10.1093/icb/42.2.319.
  • Mayle B, Ferryman M, Pepper H. 2007. Controlling grey squirrel damage to woodlands. UK: Forestry Commission; pp. 1–16.
  • Meira CS, Barbosa-Filho JM, Lanfredi-Rangel A, Guimarães ET, Moreira DRM, Soares MBP. 2016. Antiparasitic evaluation of betulinic acid derivatives reveals effective and selective anti-Trypanosoma cruzi inhibitors. Exp Parasitol. 166:108–115. doi:10.1016/j.exppara.2016.04.007.
  • Miquelle DG, Van Ballenberghe V. 1989. Impact of bark stripping by Moose on Aspen-Spruce communities. J Wildl Manage. 53(3):577–586. doi:10.2307/3809179.
  • Mitchell B, Staines B, Welch D. 1977. Ecology of Red Deer: a research review relevant to their management in Scotland. Cambridge: Institute of Terrestrial Ecology.
  • Moeck HA, Wood DL, Lindahl KQ. 1981. Host selection behavior of bark beetles (Coleoptera: scolytidae) attacking pinus ponderosa, with special emphasis on the western pine beetle, dendroctonus brevicomis. J Chem Ecol. 7(1):49–83. doi:https://doi.org/10.1007/BF00988635.
  • Morow K. 1976. Food habits of Moose from Augustów Forest of their range in certain regions of the country brought about serious acquire economic importance in forest management. Acta Theriol (Warsz). 21:101–116.
  • Mountford EP. 1997. A decade of grey squirrel bark-stripping damage to beech in Lady Park Wood, UK. Forestry. 70(1):17–29. doi:https://doi.org/10.1093/forestry/70.1.17.
  • Müller-Schwarze D, Schulte BA, Sun L, Müller-Schwarze A, Müller-Schwarze C. 1994. Red maple (Acer rubrum) inhibits feeding by beaver (Castor canadensis). J Chem Ecol. 20(8):2021–2034. doi:https://doi.org/10.1007/BF02066240.
  • Nevřelová M, Ruzickova J. 2015. Woody plants affected by ungulates in winter period, impacts and bark renewal. Ekológia (Bratislava). 34(3):235–248. doi:10.1515/eko-2015-0023.
  • Niinemets Ü, Loreto F, Reichstein M. 2004. Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends Plant Sci. 9(4):180–186. doi:https://doi.org/10.1016/j.tplants.2004.02.006.
  • Niklas KJ. 1999. The mechanical role of bark. Am J Bot. 86(4):465–469. doi:https://doi.org/10.2307/2656806.
  • Nolte DL, Kimball BA, Perry KR, Villalba JJ, Provenza FD, Johnston JJ. 2004. Development of a high performance liquid chromatography/mass spectroscopy method for the determination of strychnine concentrations in insects used to assess potential risks to insectivores. J Chromatogr B Analyt Technol Biomed Life Sci. 811(2):257–262. Proc Vertebr Pest Conf 21. doi:10.1016/j.jchromb.2004.09.009.
  • Özgenç O, Durmaz S, Çelik G, Korkmaz B, Yaylı N. 2017. Comparative phytochemical analysis of volatile organic compounds by SPME-GC-FID/MS from six coniferous and nine deciduous tree bark species grown in Turkey. South African J Bot. 113:23–28. doi:10.1016/j.sajb.2017.07.004.
  • Palo RT. 1984. Distribution of birch (Betula Spp.), willow (Salix Spp.), and poplar (Populus Spp.) secondary metabolites and their potential role as chemical defense against herbivores. J Chem Ecol. 10:499–520. doi:10.1007/BF00988096.
  • Patočka J. 2012. Biologically active pentacyclic triterpenes and their current medicine signification. J Appl Biomed. 1(1):7–12. doi:https://doi.org/10.32725/jab.2003.002.
  • Pepper HW. 1998. The prevention of rabbit damage to trees in woodland. Edinburgh: Forestry Commisssion.
  • Pulliainen E, Tunkkari PS. 1987. Winter diet, habitat selection and fluctuation of a mountain Hare Lepus timidus population in Finnish Forest Lapland. Ecography 10:261–267.
  • Quine CP, Gardiner BA. 2010. Understanding how the interaction of wind and trees results in wind-throw, stem break-age, and canopy gap formation. In: Johnson E, Miyanishi K, editors. Plant disturbance ecology: the process and the Response. 2nd ed. London: Elsevier. p. 103–155.
  • Raffa KF, Andersson MN, Schlyter F. 2016. Host selection by bark beetles: playing the odds in a high-stakes game. In: Tittiger C, Blomquist G, editors. Advances in insect physiology. Vol. 50. Oxford: Academic Press; p. 1–74.
  • Raffa KF, Grégoire JC, Lindgren BS. 2015. Natural history and ecology of Bark Beetles. In: Vega F Hofstetter R, editors. Bark Beetles: biology and ecology of native and invasive species. Oxford: Academic Press; pp. 1–40.
  • Räsänen RM, Hieta JP, Immanen J, Nieminen K, Haavikko R, Yli-Kauhaluoma J, Kauppila TJ. 2019. Chemical profiles of birch and alder bark by ambient mass spectrometry. Anal Bioanal Chem. 411(28):7573–7583. doi:https://doi.org/10.1007/s00216-019-02171-9.
  • Rayden TJ, Savill PS. 2004. Damage to beech woodlands in the Chilterns by the grey squirrel. Forestry. 77:249–253. doi:10.1093/forestry/77.3.249.
  • Renecker LA, Hudson RJ. 1985. Estimation of dry matter intake of free-ranging Moose. J Wildl Manage. 49(3):785–792. doi:https://doi.org/10.2307/3801712.
  • Rivals F, Lister AM. 2016. Dietary flexibility and niche partitioning of large herbivores through the Pleistocene of Britain. Quat Sci Rev. 146:116–133. doi:10.1016/j.quascirev.2016.06.007.
  • Rivals F, Semprebon G, Lister A. 2012. An examination of dietary diversity patterns in Pleistocene proboscideans (Mammuthus, Palaeoloxodon, and Mammut) from Europe and North America as revealed by dental microwear. Quat Int. 255:188–195. doi:10.1016/j.quaint.2011.05.036.
  • Roppolo DJ, Miller RW. 2001. Factors predisposing urban trees to sunscald. J Arboric. 27:246–254.
  • Rowe JJ. 1985. The susceptibility of tree species to bark-stripping damage by grey squirrel (Sciurus carolinensis) in England and Wales. Q J for. 79:183–190.
  • Schmitt MH, Shuttleworth A, Ward D, Shrader AM. 2018. African elephants use plant odours to make foraging decisions across multiple spatial scales. Anim Behav. 141:17–27. doi:10.1016/j.anbehav.2018.04.016.
  • Šiman P, Filipová A, Tichá A, Niang M, Bezrouk A, Havelek R, Bach H. 2016. Effective method of purification of betulin from birch bark: the importance of its purity for scientific and medicinal use. PLoS One. 11(5):e0154933. doi:https://doi.org/10.1371/journal.pone.0154933.
  • Springthorpe G, Myhill N. 1994. Wildlife rangers handbook. London (UK): Forestry Commission.
  • Stults DZ, Axsmith BJ. 2009. Betulaceae from the Pliocene and Pleistocene of Southwest Alabama, Southeastern United States. Rev Palaeobot Palynol. 155(1–2):25–31. doi:https://doi.org/10.1016/j.revpalbo.2009.01.001.
  • Stutz RS, Banks PB, Dexter N, McArthur C. 2015. Herbivore search behaviour drives associational plant refuge. Acta Oecologica. 67:1–7. doi:10.1016/j.actao.2015.05.004.
  • Stutz RS, Croak BM, Leimar O, Bergvall UA. 2017a. Borrowed plant defences: deterring browsers using a forestry by-product. For Ecol Manage. 390:1–7. doi:10.1016/j.foreco.2017.01.013.
  • Stutz RS, Croak BM, Proschogo N, Banks PB, McArthur C. 2017b. Olfactory and visual plant cues as drivers of selective herbivory. Oikos. 126(2). doi:https://doi.org/10.1111/oik.03422.
  • Sullivan TP. 1992. Tree squirrels, Woodrats and beaver. In: Black H, editor. Silvicultural approaches to animal damage in Pacific Northwest forests, Portland (OR): United States Forest Service, Pacific Northwest Research Station; Vol. 287, pp. 271–288.
  • Tenneson C, Oring L. 1985. Winter food preferences of Porcupines. J Wildl Manage. 49(1):28–33. doi:https://doi.org/10.2307/3801835.
  • Vakkari P 2009. EUFORGEN: Technical Guidelines for genetic conservation and use of silver birch (Betula pendula).
  • Verheyden H, Ballon P, Bernard V, Saint-Andrieux C. 2006. Variations in bark-stripping by red deer Cervus elaphus across Europe. Mamm Rev. 36(3):217–234. doi:https://doi.org/10.1111/j.1365-2907.2006.00085.x.
  • Vospernik S. 2006. Probability of bark stripping damage by red deer (Cervus elaphus) in Austria. Silva Fenn. 40(4):589–601. doi:https://doi.org/10.14214/sf.316.
  • Vourc’h G, De Garine-Wichatitsky M, Labbé A, Rosolowski D, Martin JL, Fritz H. 2002. Monoterpene effect on feeding choice by deer. J Chem Ecol. 28(12):2411–2427. doi:https://doi.org/10.1023/A:1021423816695.
  • Welch D, Scott D, Staines BW. 1997. Bark stripping damage by red deer in a Sitka spruce forest in western Scotland III. Trends in wound condition. Forestry. 70:113–120. doi:10.1093/forestry/70.2.113-a.
  • Wertheim A. 2010. Visual conspicuity: a new simple standard, its reliability, validity and applicability. Ergonomics. 53(3):421–442. doi:https://doi.org/10.1080/00140130903483705.
  • Wiley RH. 2006. Signal detection and animal communication. Adv Study Behav. 36:217–247.
  • Yansa CH, Adams KM. 2012. Mastodons and mammoths in the Great Lakes Region, USA and Canada: new insights into their diets as they neared extinction. Geogr Compass. 6(4):175–188. doi:10.1111/j.1749-8198.2012.00483.x.
  • Yin J, Ren CL, Zhan YG, Li CX, Xiao JL, Qiu W, Li XY, Peng HM. 2012. Distribution and expression characteristics of triterpenoids and OSC genes in white birch (Betula platyphylla suk.). Mol Biol Rep. 39(3):2321–2328. doi:https://doi.org/10.1007/s11033-011-0982-0.
  • Zidar J 2011. Factors affecting bark-stripping by red deer (Cervus elaphus) – the importance of landscape structure and forage availability [ masters thesis]. Grimso: Swedish University of Agricultural Sciences.
  • Zielke L, Wrage-Mönnig N, Müller J, Neumann C. 2019. Implications of spatial habitat diversity on diet selection of European Bison and Przewalski´s horses in a rewilding Area. Diversity. 11(4):63. doi:https://doi.org/10.3390/d11040063.