Abstract
Specimens from zoological collections play a pivotal role in improving scientific knowledge in many natural science disciplines. To guarantee an optimum state of conservation and ensure their usefulness, the preparation process employed is crucial. Skins and skeletons are key elements in vertebrate scientific collections and, ideally, are prepared from recently deceased animals; however, specimens are often stored in a frozen state for a long time (years) prior to preparation. Whether the duration of this frozen state has a deleterious effect on preparation quality has rarely been studied. The main objective of this study was thus to contribute towards research into zoological preparation by testing to see whether prolonged frozen storage hinders the preparation of bird skins and skeletons. We used the common buzzard (Buteo buteo) and the barn owl (Tyto alba) as biological models. Our results showed that long-term frozen storage led to weight loss, bone marrow acidification and solidification, and hampered skin preparation. The necropsy affected weight loss and decreased the skin tear resistance, probably due to tissue dehydration. Thus, prolonged frozen storage appears to have a harmful effect on the preparation quality of vertebrate specimens. Since frozen storage could ultimately have an impact on the conservation and scientific use of museum specimens, practices should be implemented to minimise the amount of time specimens are frozen or to mitigate any detrimental effects. More importance should be attached to research on zoological preparation since it is fundamental for optimising the quality, conservation status, and value of museum collections.
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References
Beck LA (2018) Zoological collections of Germany: the animal kingdom in its amazing plenty at museums and universities. Cham: Springer
Bergh J-E, Jensen K-MV, Åkerlund M, Stengård Hansen L, Andrén M (2006) A contribution to standards for freezing as a pest control method for museums. Collect Forum 21:117–125
Blasco R, Rosell J, Arilla M, Margalida A, Villalba D, Gopher A, Barkai R (2019) Bone marrow storage and delayed consumption at Middle Pleistocene Qesem Cave, Israel (420 to 200 ka). Sci Adv 5:eaav9822. https://doi.org/10.1126/sciadv.aav9822
Calvelo A (1981) Recent studies on meat freezing. In: Lawrie R (ed) Developments in meat science–vol. 2. London: Applied Science Publishers, pp 125–158
Campañone LA, Salvadori VO, Mascheroni RH (2005) Food freezing with simultaneous surface dehydration: approximate prediction of weight loss during freezing and storage. Int J Heat Mass Transf 48:1195–1204. https://doi.org/10.1016/j.ijheatmasstransfer.2004.09.031
Campbell BA, Baars C (2019) The curation and care of museum collections. New York: Routledge
Cano-Muñoz G (1991) Manual on meat cold store operation and management–issue 92 of FAO animal production and health paper. Rome: Food and Agriculture Organization of the United Nations
Canoville A, Schweitzer MH, Zanno LE (2019) Systemic distribution of medullary bone in the avian skeleton: ground truthing criteria for the identification of reproductive tissues in extinct Avemetatarsalia. BMC Evol Biol 19:71. https://doi.org/10.1186/s12862-019-1402-7
Carrillo-Ortiz J, Guallar S, Martínez-Vargas J, Quesada J (2021) A revision of bird skin preparation aimed at improving the scientific value of ornithological collections. Avian Biol Res 1758155920987151. https://doi.org/10.1177/1758155920987151
Cato PS, Jones C (1991) Natural history museums: directions for growth. Lubbock: Texas Tech University Press
Compagno LJV (2001) Sharks of the world: an annotated and illustrated catalogue of shark species known to date, Issue 1, Part 2. Rome: Food and Agriculture Organization of the United Nations
Corrieri B, Márquez-Grant N (2015) What do bones tell us? The study of human skeletons from the perspective of forensic anthropology. Sci Prog 98:391–402. https://doi.org/10.3184/003685015X14470674934021
Csuti B (1980) Type specimens of recent mammals in the Museum of Vertebrate Zoology, University of California. Berkeley: University of California Press
Deeth HC, Fitz-Gerald CH (2006) Lipolytic enzymes and hydrolytic rancidity. In: Fox PF, McSweeney PLH (eds) Advanced dairy chemistry–vol. 2: lipids, 3rd edn. New York: Springer, pp 481–556
Doucet SM, Hill GE (2009) Do museum specimens accurately represent wild birds? A case study of carotenoid, melanin, and structural colours in long-tailed manakins Chiroxiphia linearis. J Avian Biol 40:146–156. https://doi.org/10.1111/j.1600-048X.2009.03763.x
Edwards HGM, Gniadecka M, Petersen S, Hart Hansen JP, Faurskov Nielsen O, Christensen DH, Wulf HC (2002) NIR-FT Raman spectroscopy as a diagnostic probe for mummified skin and nails. Vib Spectrosc 28:3–15. https://doi.org/10.1016/S0924-2031(01)00141-2
Elias PM, Menon GK (1991) Structural and lipid biochemical correlates of the epidermal permeability barrier. Adv Lipid Res 24:1–26. https://doi.org/10.1016/B978-0-12-024924-4.50005-5
EURING–The European Union for Bird Ringing (2010) The EURING Exchange Code 2000 Plus. On-line Code Tables. Thetford, U.K. http://www.euring.org/data-and-codes/euring-codes. Accessed 18 Jan 2021
Fonseca DM, Campbell S, Crans WJ, Mogi M, Miyagi I, Toma T, Bullians M, Andreadis TG, Berry RL, Pagac B, Sardelis MR, Wilkerson RC (2001) Aedes (Finlaya) japonicus (Diptera: Culicidae), a newly recognized mosquito in the United States: analyses of genetic variation in the United States and putative source populations. J Med Entomol 38:135–146. https://doi.org/10.1603/0022-2585-38.2.135
Fung YC (1981) Biomechanics: mechanical properties of living tissues. New York: Springer-Verlag
Gurevitch O, Slavin S, Feldman AG (2007) Conversion of red bone marrow into yellow–cause and mechanisms. Med Hypotheses 69:531–536. https://doi.org/10.1016/j.mehy.2007.01.052
Gustafson ME, Hildenbrand J, Metras L (1997) The North American Bird Banding Manual (Electronic Version). Version 1.0. https://www.pwrc.usgs.gov/bbl/manual/. Accessed 18 Jan 2021
Hayes T, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A (2002) Feminization of male frogs in the wild. Nature 419:895–896. https://doi.org/10.1038/419895a
Hellberg ME, Bach DP, Roy K (2001) Climate-driven range expansion and morphological evolution in a marine gastropod. Science 292:1707–1710. https://doi.org/10.1126/science.1060102
Hendry D (1999) Vertebrates. In: Carter D, Walker A (eds) Care and conservation of natural history collections. Oxford: Butterworth Heinemann, pp 1–36
Herren RV (2012) Science of animal agriculture, 4th edn. New York: Cengage Learning
Hildebrand M (1968) Anatomical preparations. Berkeley: University of California Press
Holmes MW, Hammond TT, Wogan GOU, Walsh RE, LaBarbera K, Wommack EA, Martins FM, Crawford JC, Mack KL, Bloch LM, Nachman MW (2016) Natural history collections as windows on evolutionary processes. Mol Ecol 25:864–881. https://doi.org/10.1111/mec.13529
Horie CV (1990) Deterioration of skin in museum collections. Polym Degrad Stab 29:109–133. https://doi.org/10.1016/0141-3910(90)90025-3
Kennedy CJ (2000) Managing frozen foods. Cambridge: Woodhead Publishing Limited
Kennedy EA (2010) Color variation in museum specimens of birds: effects of stress, pigmentation, and duration of storage. Dissertation, Bucknell University
Kite M, Thomson R (2006) Conservation of leather and related materials. Oxford: Butterworth-Heinemann
Knox A (1980) Post-mortem changes in wing-lengths and wing-formulae. Ringing Migr 3:29–31. https://doi.org/10.1080/03078698.1980.9673758
Kuczyński L, Tryjanowski P, Antczak M, Skoracki M, Hromada M (2002) Repeatability of measurements and shrinkage after skinning: the case of the Great Grey Shrike Lanius excubitor. Bonn Zool Beitr 51:127–130
Laitinen M, Kivikari R, Hirn M (2006) Lipid oxidation may reduce the quality of a fresh frozen bone allograft. Is the approved storage temperature too high? Acta Orthop 77:418–421. https://doi.org/10.1080/17453670610046343
Lamichhaney S, Card DC, Grayson P, Tonini JFR, Bravo GA, Näpflin K, Termignoni-Garcia F, Torres C, Burbrink F, Clarke JA, Sackton TB, Edwards SV (2019) Integrating natural history collections and comparative genomics to study the genetic architecture of convergent evolution. Philos Trans R Soc B 374:20180248. https://doi.org/10.1098/rstb.2018.0248
Lanir Y, Fung YC (1974) Two-dimensional mechanical properties of rabbit skin–II Experimental results. J Biomech 7:171–182. https://doi.org/10.1016/0021-9290(74)90058-X
Lees S, Bonar LC, Mook HA (1984) A study of dense mineralized tissue by neutron diffraction. Int J Biol Macromol 6:321–326. https://doi.org/10.1016/0141-8130(84)90017-5
Leirs H, Mills JN, Krebs JW, Childs JE, Akaibe D, Woollen N, Ludwig G, Peters CJ, Ksiazek TG (1999) Search for the Ebola virus reservoir in Kikwit, Democratic Republic of the Congo: reflections on a vertebrate collection. J Infect Dis 179:S155–S163. https://doi.org/10.1086/514299
Lievers WB, Poljsak AS, Waldman SD, Pilkey AK (2010) Effects of dehydration-induced structural and material changes on the apparent modulus of cancellous bone. Med Eng Phys 32:921–925. https://doi.org/10.1016/j.medengphy.2010.06.001
Lyman RL (2010) Paleozoology’s dependence on natural history collections. J Ethnobiol 30:126–136. https://doi.org/10.2993/0278-0771-30.1.126
MacDonald S, Ashby J (2011) Museums: campus treasures. Nature 471:164–165. https://doi.org/10.1038/471164a
Marte F, Péquignot A, von Endt DW (2006) Arsenic in taxidermy collections: history, detection, and management. Collect Forum 21:143–150
Marti CD (1994) Barn owl reproduction: patterns and variation near the limit of the species’ distribution. Condor 96:468–484. https://doi.org/10.2307/1369329
Mathias J (1994) Housing and maintenance of collections. In: Stansfield G, Mathias J, Reid G (eds) Manual of natural history curatorship. London: H.M. Stationery Office, pp 98–143
McDonald HG (2006) Vertebrate skeletons: preparation and storage. Conserve O Gram 11(7):1–8
McLelland J (1992) Atlas en color de anatomía de las aves. Madrid: Interamericana–McGraw-Hill
Menon GK, Maderson PFA, Drewes RC, Baptista LF, Price LF, Elias PM (1996) Ultrastructural organization of avian stratum corneum lipids as the basis for facultative cutaneous waterproofing. J Morphol 227:1–13. https://doi.org/10.1002/(SICI)1097-4687(199601)227:1%3c1::AID-JMOR1%3e3.0.CO;2-F
Miller GE, Grant PM, Kishnore R, Steinkruger FJ, Rowland FS, Guinn VP (1972) Mercury concentrations in museum specimens of tuna and swordfish. Science 175:1121–1122. https://doi.org/10.1126/science.175.4026.1121
Miralles A, Bruy T, Wolcott K, Scherz MD, Begerow D, Beszteri B, Bonkowski M, Felden J, Gemeinholzer B, Glaw F, Glöckner FO, Hawlitschek O, Kostadinov I, Nattkemper TW, Printzen C, Renz J, Rybalka N, Stadler M, Weibulat T, Wilke T, Renner SS, Vences M (2020) Repositories for taxonomic data: where we are and what is missing. Syst Biol syaa026. https://doi.org/10.1093/sysbio/syaa026
Mularchuk P, Boskey A (1990) Lipids in bone: optimal conditions for tissue storage prior to lipid analyses. Calcif Tissue Int 46:57–59. https://doi.org/10.1007/BF02555825
Murmann DC, Brumit PC, Schrader BA, Senn DR (2006) A comparison of animal jaws and bite mark patterns. J Forensic Sci 51:846–860. https://doi.org/10.1111/j.1556-4029.2006.00166.x
Nattier R (2018) Biodiversity in natural history collections: a source of data for the study of evolution. In: Grandcolas P, Maurel M-C (eds) Biodiversity and evolution. London: ISTE Press – Elsevier, pp 175–187
Nikolaeva LP (2018) Features of acid-base balance of bone marrow. Acta Medica Int 5:55–57. https://doi.org/10.4103/ami.ami_80_17
Nyman JS, Roy A, Shen X, Acuna RL, Tyler JH, Wang X (2006) The influence of water removal on the strength and toughness of cortical bone. J Biomech 39:931–938. https://doi.org/10.1016/j.jbiomech.2005.01.012
Orta C, Roqué L (2011) Protocol de preparació de pells planes de mamífers, aus o rèptils–animal sencer o parcial. Museu de Ciències Naturals de Barcelona. Unpublished document
Orta C, Roqué L, Blanco À (2011) Protocol de preparació d’esquelets desarticulats en KOH. Museu de Ciències Naturals de Barcelona. Unpublished document
Ozawa S, Koishikawa T, Chikuni K, Yoshitake M (1990) Effect of slaughter body weight on postmortem changes in pH value, glycogen, lactic acid and nucleotides of longissimus muscle in Holstein steers. Jpn J Zootech Sci 61:385–389
Parmesan C, Ryrholm N, Stefanescu C, Hill JK, Thomas CD, Descimon H, Huntley B, Kaila L, Kullberg J, Tammaru T, Tennent WJ, Thomas JA, Warren M (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579–583. https://doi.org/10.1038/21181
Péquignot A (2006) The history of taxidermy: clues for preservation. Collect J Mus Arch Prof 2:245–255. https://doi.org/10.1177/155019060600200306
Péquignot A, Tumosa CS, von Endt DW (2006) The effects of tanning and fixing processes on the properties of taxidermy skins. Collect Forum 21:133–142
Pham QT, Mawson RF (1997) Moisture migration and ice recrystallization in frozen foods. In: Erickson MC, Hung YC (eds) Quality in frozen food. Boston: Springer, pp 67–91
Pohland G, Mullen P (2006) Preservation agents influence UV-coloration of plumage in museum bird skins. J Ornithol 147:464–467. https://doi.org/10.1007/s10336-005-0038-0
Quevedo F, Hernández-Camacho J, Muñoz-Saba Y, Simmons JE (2005) Curtiembre de pieles. In: Simmons JE, Muñoz-Saba Y (eds) Cuidado, manejo y conservación de las colecciones biológicas. Bogotá: Universidad Nacional de Colombia, pp 76–88
Ratcliffe DA (1967) Decrease in eggshell weight in certain birds of prey. Nature 215:208–210. https://doi.org/10.1038/215208a0
Ravindran S, Saufi S, Amni WN, Ishak I, Hamid NH, Abidin CMRZ, Ahmad AH, Azzam G, Salim H (2018) Sex identification comparison of barn owls (Tyto alba javanica) using morphological features and molecular-based methods. Slovak Raptor J 12:47–54. https://doi.org/10.2478/srj-2018-0005
Ruane S, Austin CC (2017) Phylogenomics using formalin-fixed and 100+ year-old intractable natural history specimens. Mol Ecol Resour 17:1003–1008. https://doi.org/10.1111/1755-0998.12655
Sandoval Salinas ML, Sandoval JD, Colombo EM, Barquez RM (2018) The pattern of color change in small mammal museum specimens: is it independent of storage histories given museum-specific conditions? BMC Res Notes 11:424. https://doi.org/10.1186/s13104-018-3544-x
Simmons JE, Snider J (2012) Observation and distillation—preservation, depiction, and the perception of nature. Bibl Herpetol 9:115–134
Simmons NB, Voss RS (2009) Collection, preparation, and fixation of specimens and tissues. In: Kunz TH, Parsons S (eds) Ecological and behavioral methods for the study of bats, 2nd edn. Baltimore: Johns Hopkins University Press, pp 849–864
Staniforth S (1984) Environmental conservation. In: Thompson JMA (ed) Manual of curatorship: a guide to museum practice. London: Butterworths, pp 192–202
StatSoft, Inc. (2014) STATISTICA (data analysis software system), version 12. Tulsa, OK
Suarez AV, Tsutsui ND (2004) The value of museum collections for research and society. Bioscience 54:66–74. https://doi.org/10.1641/0006-3568(2004)054[0066:TVOMCF]2.0.CO;2
Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. Proc Natl Acad Sci USA 98:1095–1100. https://doi.org/10.1073/pnas.98.3.1095
Tétreault J (2017) Products used in preventive conservation. Ottawa: Canadian Conservation Institute
Tiee MS, Harrigan RJ, Thomassen HA, Smith TB (2018) Ghosts of infections past: using archival samples to understand a century of monkeypox virus prevalence among host communities across space and time. Royal Soc Open Sci 5:171089. https://doi.org/10.1098/rsos.171089
Töpfer T, Gamauf A, Haring E (2011) Utility of arsenic-treated bird skins for DNA extraction. BMC Res Notes 4:197. https://doi.org/10.1186/1756-0500-4-197
Tortora GJ, Funke BR, Case CL (2019) Microbiology: an introduction, 13th edn. San Francisco: Pearson Benjamin Cummings
Tsangaras K, Greenwood AD (2012) Museums and disease: using tissue archive and museum samples to study pathogens. Ann Anat 194:58–73. https://doi.org/10.1016/j.aanat.2011.04.003
Viscardi P, Sigwart JD, Monaghan NT (2006) Climate control in an uncontrollable building. Collect Forum 21:85–95
Wazir H, Chay SY, Zarei M, Hussin FS, Mustapha NA, Wan Ibadullah WZ, Saari N (2019) Effects of storage time and temperature on lipid oxidation and protein co-oxidation of low-moisture shredded meat products. Antioxidants 8:486. https://doi.org/10.3390/antiox8100486
White CL, Dusek RJ (2015) Wildlife specimen collection, preservation, and shipment. In: Franson JC, Friend M, Gibbs SEJ, Wild MA (eds) Field manual of wildlife diseases: U.S. Geological Survey Techniques and Methods 15–C4
Williams SL, Hawks CA (1987) History of preparation materials used for recent mammal specimens. In: Genoways HH, Jones C, Rossolimo OL (eds) Mammal collection management. Lubock: Texas Tech University Press, pp 21–49
Windsor P, Pinniger D, Bacon L, Child B, Harris K (2015) Integrated pest management for collections-Proceedings of 2011: a pest odyssey, 10 years later. Swindon: English Heritage
Winker K (2000) Obtaining, preserving, and preparing bird specimens. J Field Ornithol 71:250–297. https://doi.org/10.1648/0273-8570-71.2.250
Winker K (2004) Natural history museums in a postbiodiversity era. Bioscience 54:455–459. https://doi.org/10.1641/0006-3568(2004)054[0455:NHMIAP]2.0.CO;2
Yang W, Sherman VR, Gludovatz B, Schaible E, Stewart P, Ritchie RO, Meyers MA (2015) On the tear resistance of skin. Nat Commun 6:6649. https://doi.org/10.1038/ncomms7649
Zaritzky NE (2008) Frozen storage. In: Evans JA (ed) Frozen food science and technology. Oxford: Blackwell Publishing Ltd, pp 224–247
Zhou X, Zhou D-Y, Liu Z-Y, Yin F-W, Liu Z-Q, Li D-Y, Shahidi F (2018) Hydrolysis and oxidation of lipids in mussel Mytilus edulis during cold storage. Food Chem 272:109–116. https://doi.org/10.1016/j.foodchem.2018.08.019
Acknowledgements
We would like to thank Enric Ruíz, Lleonard Barrios, Lluís Puig, Albert Burgas, and Xavier Larruy for their contributions to this study. We are also grateful to Marta Pérez-Azcárate and Michael Lockwood, who made interesting comments on an earlier version of this manuscript.
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This work was financially supported by the Natural Science Museum of Barcelona (JQ) and the Ministry of Economy and Competitiveness (grant number PTA 2014–09302-I; JC-O).
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Study conception and design: JQ, LR, CO; development of methodology: JQ, CO, IdC, LR, JC-O; material preparation and data collection: LR; formal analysis of the study data: JQ, JM-V, JC-O; drafting of the manuscript: JM-V, JC-O, IdC, JQ; critical revision of the manuscript: JM-V, JQ; research supervision and project administration: JQ. All authors read and approved the final manuscript.
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Martínez-Vargas, J., Roqué, L., del Canto, I. et al. The impact of prolonged frozen storage on the preparation quality of bird skins and skeletons in zoological collections. Sci Nat 108, 18 (2021). https://doi.org/10.1007/s00114-021-01726-0
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DOI: https://doi.org/10.1007/s00114-021-01726-0