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Temporal Change in Fur Color in Museum Specimens of Mammals: Reddish-Brown Species Get Redder with Storage Time

Temporal Change in Fur Color in Museum Specimens of Mammals: Reddish-Brown Species Get Redder... Hindawi Publishing Corporation International Journal of Zoology Volume 2013, Article ID 876347, 6 pages http://dx.doi.org/10.1155/2013/876347 Research Article Temporal Change in Fur Color in Museum Specimens of Mammals: Reddish-Brown Species Get Redder with Storage Time 1 1 1 Andrew K. Davis, Natalie Woodall, Jake P. Moskowitz, 2 2 Nikole Castleberry, and Byron J. Freeman Odum School of Ecology, The University of Georgia, Athens, GA 30602, USA Georgia Museum of Natural History, The University of Georgia, Athens, GA 30602, USA Correspondence should be addressed to Andrew K. Davis; akdavis@uga.edu Received 25 March 2013; Accepted 13 May 2013 Academic Editor: Randy J. Nelson Copyright © 2013 Andrew K. Davis et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Museum collections have great value for zoological research, but despite careful preservation, over time specimens can show subtle changes in color. We examined the eeff ct of storage time on fur color of two reddish-brown species, golden mice ( Ochrotomys nuttalli) and eastern chipmunk (Tamias striatus). Using image analysis, we obtained color data (hue, saturation, and density) on 91 golden mice and 49 chipmunks from Georgia, USA. Analyses that considered body size, gender, and collection year showed significant eeff cts of year on fur color of golden mice (hue and saturation) and of agouti color of chipmunks. Older specimens tended to be redder in color than newer specimens, consistent with a prior study of red bats (Lasiurus borealis). Hair samples showed reddening of fine body hairs, but not in thicker guard hairs. There was no temporal change in black or white stripe color in chipmunks, indicating that this temporal eeff ct would be limited to species with reddish-brown fur. This eeff ct may be caused by breakdown of eumelanin pigments (which make dark colors) over time, leaving a greater proportion of pheomelanin pigments (which make red colors). eTh se results show that storage time needs to be considered in research projects where fur color is of importance. 1. Introduction museum exhibits. However, these bat specimens had always been housed in drawers within standard metal museum Museum collections of animals have always been a valuable cabinets (i.e., in darkness). At the time, it was thought that resource for zoological research. Older specimens in par- this was from breakage of buffy-tipped hair b fi res on older ticular offer insights into the past and allow researchers to specimens.Sincethatstudy,wehaveexaminedtwoadditional track the historical incidence of deformities [1], document mammal species in this same museum to look for evidence of species declines [2], and extract DNA for genetic analyses [3]. temporal color changes in their fur, and we report the results An implicit assumption with all museum collections is that of these investigations here. once a specimen is added to a collection and properly stored, Aside from the previous study, there have been no it remains unchanged through time. In a recent museum previous investigations of mammalian pelage color in study of pelage color in red bats (Lasiurus borealis), a curious museum collections. In contrast, numerous investigators discovery was made, where older specimens tended to have have searched for temporal changes in coloration of birds redder shades of pelage than did newer specimens [4], which in museum collections, with varying results [7, 8]. While is the opposite patter one would expect if specimens simply many of these studies focused on the bright carotenoid-based faded over time. Indeed, color fading does happen when pigments of bird feathers, one study also examined the black specimens (of most taxa) are exposed to light [5, 6]suchasin (melanin-based) color of bird specimens [9], and these results 2 International Journal of Zoology Average hue, saturation (a) (c) (e) Average hue, saturation Average hue, saturation Average density (b) (d) (f ) Figure 1: Photographs of the two species studied, golden mouse (a) an d chipmunk (b), and method of measuring color from photographs. Specimens were photographed ((c) and (d)), and image analysis software was used to measure fur color in the selected areas ((e) and (f); see Section 2 for color measurement). eTh agouti, white, and black stripes of chipmunks (f) were measured separately. Rump color (green box in (d)) was also measured in chipmunks. Photo credits: Josh Campbell (a) and Richard Cameron (b). would be helpful for comparison to the melanin-based color have fur that has a golden-brown or tan color throughout of mammals. Doucet and Hill [9] showed how feathers with (Figure 1(a)). The eastern chipmunk has a mixture of agouti melanin-based colors tended to have higher red chroma in and reddish-brown fur, with white and black dorsal stripes older specimens. Since all melanin-based color is formed by (Figure 1(b)). Including chipmunks in this study allowed us a combination of two melanin pigments, eumelanin (which to compare effects of storage on all fur colors (agouti, black, makes dark colors) and pheomelanin (which makes yellow to white, and red). Results of this investigation will bear on all redcolors),theyspeculatedthateumelanin maybemoresus- projects where color of mammal skins is of importance and ceptible to degradation than pheomelanin pigments, which moreover will further enhance understanding of the eeff cts of over time couldleadtoreduced proportionsofthispigment long-term storage on animal tissues. in the feathers, ultimately resulting in higher reflectance at longer wavelengths (i.e., giving the feathers a slightly reddish color). This is in agreement with at least one anecdotal 2. Methods account from a seasoned museum curator who indicated that of the two melanin pigments, eumelanin tends to become 2.1. Museum Specimens. Specimens of each species were paler and redder over time, while pheomelanin becomes paler obtained from the Georgia Museum of Natural History, in with age (personal communication cited in [10]). Athens, GA (USA). While this museum holds specimens Ourprimary objectiveofthe currentstudy wasto from throughout the southeastern United States, we limited determine if the temporal change in color seen in the our analyses here to animals from the State of Georgia, previous red bat study [4] could be seen in other species to minimize the possibility of comparing different races or (with reddish-brown fur) in museum collections. The species animals that may be locally adapted to differing climates. examined were golden mouse (Ochrotomys nuttalli)and east- eTh collection of golden mice from Georgia contained 91 ern chipmunk (Tamias striatus), which both are native to the specimens that had been collected between 1935 and 1996. United States (although we only examined specimens from The eastern chipmunk collection from Georgia consisted of Georgia; see Section 2). As their name suggests, golden mice 49 specimens collected between 1946 and 1996. All had been International Journal of Zoology 3 prepared in a similar manner, that is, as skins placed in a distributed, based on visual inspection of their frequency standardized position (see Figure 1), and with no chemicals distributions. We therefore used General Linear Modeling or preservatives applied to the pelage. All specimens were to determine if pelage color of either species varies through stored in drawers within metal cabinets and were kept as time. For the golden mice, both hue and saturation were used such, as well as in complete darkness, for the entirety of their as dependent variables, gender was a predictor, and body storage life. From the information on the specimen tags, we size (i.e., total length) and collection year were covariates. A recorded the gender and total length of each animal prior to similar approach was used to examine color in chipmunks, photography (later). although here we separately examined each color type, including the agouti, white, and black stripes of the dorsum and the red color of the rump. All analyses were conducted 2.2. Measuring Pelage Color. Regardless of species, each using the Statistica 6.1 software package [ 14]. animal was individually positioned directly under a digital camera on a copystand and photographed (see Figure 1). The same copystand was used for both collections, but at two 3. Results separate times. Golden mice were photographed on January 1, 2011, while chipmunks were photographed on January 17, In the golden mice specimens, there was no significant effect 2013 (although actual dates and times of photography should of body size on pelage hue (𝐹 = 0.951,𝑃 = 0.332 ), nor 1,84 be meaninglessinthisstudy). Allphotography wasdonein was there a difference between males and females ( 𝐹 = 1,84 a room in the museum. In all cases, no camera flash was 0.987, 𝑃 = 0.323 ). There was a nearly significant effect used; artificial lighting was directed toward the specimen of collection year (𝐹 = 3.819,𝑃 = 0.054 ), with more 1,84 from both sides of the camera (using side-mounted lights on recent specimens tending to have larger hue scores (less red; the copystand) so at least within each collection, the lighting Figure 2(a)). eTh analysis of pelage saturation of golden mice for all specimens was standardized. This was important since showed significant variation with body size ( 𝐹 = 16.96, 1,84 we were interested only in the relative dieff rences among 𝑃<0.001 ), no effect of gender ( 𝐹 =1.82,𝑃=0.180 ), and 1,84 individuals within the mice or chipmunk collections, not in a significant relationship with collection year ( 𝐹 =13.43, 1,84 comparing mice versus chipmunk colors. 𝑃 < 0.001 ), such that more recent specimens had lower From the photographs we used image analysis proce- saturation scores (their color was less pure; Figure 2(a)). dures to quantify the degree of redness in the specimens In the analysis of dorsal agouti color in the chipmunks, [4, 11, 12]. For this, images were imported into Adobe there was no effect of body size ( 𝐹 = 0.173,𝑃 = 0.679 ) 1,42 Photoshop with FoveaPro plugins installed (http://www nor of gender (𝐹 = 0.549, 𝑃 = 0.462 )onhue,but 1,42 .reindeergraphics.com/). For the golden mice, an oval selec- a signicfi ant effect of collection year ( 𝐹 =7.71,𝑃= 1,42 tion was drawn over the dorsal surface that covered as much 0.008), with more recent specimens having higher hue scores of the furred area as possible without touching the ears (Figure 2(b)). There was no eeff ct of body size ( 𝐹 =0.087, 1,42 (Figure 1). Using a FoveaPro plugin, the average pixel hue 𝑃 = 0.769 ) or gender (𝐹 = 0.626,𝑃 = 0.433 )onthe 1,42 and saturation values of this selected area were obtained. agouti saturation scores, but a signicfi ant effect of collection With computer software, hue is measured in degrees (0–360), year (𝐹 =7.83,𝑃 = 0.007 ), with more recent specimens 1,42 with lower scores representing redder colors, while brightness having lower saturation scores (Figure 2(b)). Results of the analyses of white and black dorsal stripes on the chipmunks is measured from 0 to 255, with higher scores indicating purer colors. From the chipmunk specimens we first selected showed no eects ff of gender, body size, or collection year, a square region of the dorsal surface that encompassed the on white hue, saturation, or the black density scores (𝑃> stripedregiononthe dorsum (Figure 1), andthenwithinthis 0.1 for all predictor variables in all models). Results of the box we measured color of the agouti, black, and white stripes analyses of hue and saturation of the chipmunk rump color individually.For this,one of us traced theedgeofthe stripes were nearly identical to the analyses of agouti color (i.e., with on the left and right sides, and we obtained the hue and the same signicfi ant predictor variables) and are not reported saturation within these traced areas. For the agouti pelage here. andwhite dorsal stripes, we obtained theaverage hueand In sum, while the magnitude of the effect differed by saturation scores. For the black dorsal stripes, we obtained species, results from analyses of golden mice and chipmunk theaverage pixeldensity scoreofthe traced area,which is a color (at least for the agouti fur) were qualitatively similar; measureof“blackness” andrangesfrom0to 255, with 0being specimens from earlier years tend to be redder than those perfect black and 255 perfect white [13]. These values were from more recent years. This pattern can be visually seen obtained for the left and right sides and averaged for each when photos of representative early and later specimens of specimen. Finally, we also measured the hue and saturation each species are cropped at the region of interest (middle of of the rump of each chipmunk, which we defined as the thedorsum) andplacedside-by-side(Figure 3). region from the base of the tail to where the dorsal stripes end (Figure 1(b)). This region consists of only reddish-brown 4. Discussion fur. Results from this study are consistent with the prior inves- 2.3. Data Analyses. All pelage hue, saturation, and density tigation of red bats from Georgia (from the same museum), values of the golden mice and chipmunks were normally in which older specimens were found to be redder in color 4 International Journal of Zoology r = 0.21, P = 0.048 r = 0.44, P = 0.0017 1930 1940 1950 1960 1970 1980 1990 2000 1940 1950 1960 1970 1980 1990 2000 Collection year Collection year 240 210 r = −0.34, P = 0.0010 r = −0.3, P = 0.0358 205 150 1930 1940 1950 1960 1970 1980 1990 2000 1940 1950 1960 1970 1980 1990 2000 Collection year Collection year (a) Golden mouse (b) Chipmunk (agouti fur only) Figure 2: Relationships between storage time (collection year) and pelage color (hue and saturation) for golden mice (a) and chipmunks (b). Only the values from the agouti pelage of chipmunks are shown. There was no temporal eeff ct on the white and black stripes of chipmunks. than more recent specimens [4]. At the time, it was thought temporal pattern must be common to all three. eTh simplest that this pattern was the result of breakage of hair shaft tips explanation is that the fur of all three species undergoes in older specimens, although further examination of the bat certain biochemical changes in storage, such as breakdown of collection as well as the species considered here found no eumelanin pigment in the hair b fi ers, which was speculated evidence for hair breakage. This can be seen in digital scans by Doucet and Hill [9]. Over time this would result in greater of hair samples (of the agouti fur) taken from early and proportions of the redder pheomelanin pigment in the fur later chipmunk specimens, which show intact guard hairs and a redder overall coat color in older specimens. If this is in both cases (Figure 4). However, these scans also reveal indeed the case, it emphasizes the importance of considering that much of the color variation between older and newer storage time in research studies using mammal skins and specimens is in the fine body hair of the animals, rather than where color is of importance. the thicker guard hairs. In the older specimens, these ne fi eTh re is also the possibility that early collectors may hairs appear redder than in the newer specimens. Meanwhile, have used different methods to prepare study skins at this the thick guard hair appears unchanged. It may be that the museum, which in some cases can cause reddening of pelage thickness and size of the hair determine its susceptibility to [15]. In particular, soaking the skin in tap water to relax it color change. This could also explain why we saw no temporal prior to stuffing appears to cause pelage reddening, and this eeff ctonthe whiteand blackdorsalstripes of thechipmunks, eeff ct can be seen in most mammal species, but especially in which consist primarily of white or black guard hairs (see squirrels [15]. However, whilemostofthe collectors of the Figure 3). earliest specimens (prior to 1960) at the Georgia Museum We therefore have similar results now from three different of NaturalHistory have sincepassed, thereisconsensus mammal species from Georgia, all with distinct life histories, among the current workers that specimens have always been habitat preferences, and so forth. Because of these differences prepared here according to standard mammalogy guidelines in biology and life history, the mechanism behind the [16], which does not include soaking. Less pure Saturation Purer red More red Hue Less red Less pure Saturation Purer red More red Hue Less red International Journal of Zoology 5 1942 1993 (a) (a) 1954 1996 (b) Figure 3: Comparison of representative older and newer specimens (b) of golden mice (a) and chipmunks (b), cropped to show the region measured. Figure 4: Scans of hair samples taken from an older chipmunk specimen and a newer chipmunk specimen, to show differences in color. Hair samples were scanned on a flatbed scanner with no color correction. Samples were cut from the agouti fur on the dorsum of Results from this study lead us to wonder how prevalent the specimens. Note the red coloring of the fine body hair in the older specimen, compared to the newer specimen (white arrows) this phenomenon is in mammalian collections here and in and that there is no breakage of hair tips in the older specimen (black other museums. While our intention here was only to confirm arrows). the existence of the temporal eeff ct found in the prior study of red bats (and we therefore only chose species that had reddish fur, similar to red bats), the lack of color change found in the black and white chipmunk fur suggests that this effect may Barrett contributed helpful comments on the project and on only be observed in species with reddish fur. Moreover, it the biology of golden mice. may be that species with especially fine hairs would also be susceptibletochange(sincethe nfi ebodyhairs of chipmunks changed more than the guard hairs). References A variety of scientific investigations, spanning many [1] P. T. J. Johnson, K. B. Lunde, D. A. Zelmer, and J. K. Werner, decades, have incorporated measures of pelage color of “Limb deformities as an emerging parasitic disease in amphib- museum specimens (e.g., [17–20]). Such studies require that ians: evidence from museum specimens and resurvey data,” all specimens accurately represent their “true” color (i.e., their Conservation Biology,vol.17, no.6,pp. 1724–1737, 2003. color at the time and place of collection). Given this temporal [2] H. B. Shaeff r, R. N. Fisher, and C. Davidson, “The role of natural pattern found here, it would be wise for future investigators history collections in documenting species declines,” Trends in to consider storage time in all analyses of mammalian color, Ecology & Evolution,vol.13, no.1,pp. 27–30, 1998. especially for species with reddish-brown fur. [3] A. C. M. Junqueira, A. C. Lessinger, and A. M. L. Azeredo-Espin, “Methods for the recovery of mitochondrial DNA sequences from museum specimens of myiasis-causing flies,” Medical and Acknowledgments Veterinary Entomology,vol.16, no.1,pp. 39–45, 2002. eTh authors thank Sonia Altizer for use of lab space and [4] A.K.Davis andS.B.Castleberry,“Pelage colorofred bats Liz McGhee for assistance with obtaining specimens. Gary Lasiurus borealis varies with body size: an image analysis of 6 International Journal of Zoology museum specimens,” Current Zoology,vol.56, no.4,pp. 401– 405, 2010. [5] W. B. McKillop, “Induced colour fading in entomological specimens,” J. Waddington and D. M. Rudkin, Eds., pp. 101– 104, Proceedings of the Workshop on Care and Maintenance of Natural History Collections Royal Ontario Museum, Toronto, Canada, 1986. [6] J. Hudon, “Considerations in the conservation of feathers and hair, particularly their pigments,” in Fur Trade Legacy. eTh Preservation of Organic Materials, M. Brunn and J. A. Burns, Eds., pp. 127–147, Canadian Association for Conservation of Cultural Property, Ottawa, Canada, 2005. [7] G. D. McNett and K. Marchetti, “Ultraviolet degradation in carotenoid patches: live versus museum specimens of wood warblers (Parulidae),” Auk,vol.122,no. 3, pp.793–802,2005. [8] J. K. Armenta, P. O. Dunn, and L. A. Whittingham, “Effects of specimen age on plumage color,” Auk,vol.125,no. 4, pp.803– 808, 2008. [9] S.M.Doucet andG.E.Hill,“Do museum specimensaccurately represent wild birds? A case study of carotenoid, melanin, and structural colours in long-tailed manakins Chiroxiphia linearis,” Journal of Avian Biology,vol.40, no.2,pp. 146–156, [10] C. A. Hawks, S. L. Williams, and J. S. Gardner, The Care of Tanned Skins in Mammal Research Collections. Museology,vol. 6, Texas Tech University Publication, 1984. [11] A. K. Davis, “Wing color of monarch butterflies ( Danaus plexippus) in Eastern North America across life stages: migrants are “redder” than breeding and overwintering stages,” Psyche, vol. 2009, Article ID 705780, 5 pages, 2009. [12] A. K. Davis, J. Chi, C. A. Bradley, and S. Altizer, “The redder the better: wing color predicts flight performance in monarch butterflies,” PloS ONE,vol.7,no. 7, ArticleIDe41323, 2012. [13] A.K.Davis,B.D.Farrey, andS.Altizer,“Variationinther- mally induced melanism in monarch butterflies (Lepidoptera: Nymphalidae) from three North American populations,” Jour- nal of eTh rmal Biology , vol. 30, no. 5, pp. 410–421, 2005. [14] Statistica, Statistica Version 6. 1,Statsoft Inc.,2003. [15] S. C. Downing, “Color changes in mammal skins during preparation,” Journal of Mammalogy,vol.26, pp.128–132,1945. [16] A. F. DeBlase and R. E. Martin, “A manual of mammalogy with keys to the families of the world,” in Specimen Preparation and Preservation, chapter 35, Wm. C. Brown Company Publishers, Dubuque, Iowa, USA, 2nd edition, 1981. [17] H. H. Collins, “Studies of the pelage phases and of the nature of color variations in mice of the genus Peromyscus,” Journal of Experimental Zoology,vol.38, pp.45–107, 1923. [18] R. H. Pine,J.E.Rice, J. E. Bucher,D.H.Tank, andA.M. Greenhall, “Labile pigments and u fl orescent pelage in didelphid marsupials,” Mammalia,vol.49, pp.249–256,1985. [19] L. N. Carraway and B. J. Verts, “Geographic variation in pelage color of pino ˜ n mice (Peromyscus truei) in the northern Great Basin and environs,” Western North American Naturalist,vol.62, no. 4, pp. 458–465, 2002. [20] D. Ge,A.A.Lissovsky,L.Xia,C.Cheng,A.T.Smith,and Q. Yang, “Reevaluation of several taxa of Chinese lagomorphs (Mammalia: Lagomorpha) described on the basis of pelage phenotype variation,” Mammalian Biology,vol.77,no.2,pp.113– 123, 2012. 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Temporal Change in Fur Color in Museum Specimens of Mammals: Reddish-Brown Species Get Redder with Storage Time

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Hindawi Publishing Corporation International Journal of Zoology Volume 2013, Article ID 876347, 6 pages http://dx.doi.org/10.1155/2013/876347 Research Article Temporal Change in Fur Color in Museum Specimens of Mammals: Reddish-Brown Species Get Redder with Storage Time 1 1 1 Andrew K. Davis, Natalie Woodall, Jake P. Moskowitz, 2 2 Nikole Castleberry, and Byron J. Freeman Odum School of Ecology, The University of Georgia, Athens, GA 30602, USA Georgia Museum of Natural History, The University of Georgia, Athens, GA 30602, USA Correspondence should be addressed to Andrew K. Davis; akdavis@uga.edu Received 25 March 2013; Accepted 13 May 2013 Academic Editor: Randy J. Nelson Copyright © 2013 Andrew K. Davis et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Museum collections have great value for zoological research, but despite careful preservation, over time specimens can show subtle changes in color. We examined the eeff ct of storage time on fur color of two reddish-brown species, golden mice ( Ochrotomys nuttalli) and eastern chipmunk (Tamias striatus). Using image analysis, we obtained color data (hue, saturation, and density) on 91 golden mice and 49 chipmunks from Georgia, USA. Analyses that considered body size, gender, and collection year showed significant eeff cts of year on fur color of golden mice (hue and saturation) and of agouti color of chipmunks. Older specimens tended to be redder in color than newer specimens, consistent with a prior study of red bats (Lasiurus borealis). Hair samples showed reddening of fine body hairs, but not in thicker guard hairs. There was no temporal change in black or white stripe color in chipmunks, indicating that this temporal eeff ct would be limited to species with reddish-brown fur. This eeff ct may be caused by breakdown of eumelanin pigments (which make dark colors) over time, leaving a greater proportion of pheomelanin pigments (which make red colors). eTh se results show that storage time needs to be considered in research projects where fur color is of importance. 1. Introduction museum exhibits. However, these bat specimens had always been housed in drawers within standard metal museum Museum collections of animals have always been a valuable cabinets (i.e., in darkness). At the time, it was thought that resource for zoological research. Older specimens in par- this was from breakage of buffy-tipped hair b fi res on older ticular offer insights into the past and allow researchers to specimens.Sincethatstudy,wehaveexaminedtwoadditional track the historical incidence of deformities [1], document mammal species in this same museum to look for evidence of species declines [2], and extract DNA for genetic analyses [3]. temporal color changes in their fur, and we report the results An implicit assumption with all museum collections is that of these investigations here. once a specimen is added to a collection and properly stored, Aside from the previous study, there have been no it remains unchanged through time. In a recent museum previous investigations of mammalian pelage color in study of pelage color in red bats (Lasiurus borealis), a curious museum collections. In contrast, numerous investigators discovery was made, where older specimens tended to have have searched for temporal changes in coloration of birds redder shades of pelage than did newer specimens [4], which in museum collections, with varying results [7, 8]. While is the opposite patter one would expect if specimens simply many of these studies focused on the bright carotenoid-based faded over time. Indeed, color fading does happen when pigments of bird feathers, one study also examined the black specimens (of most taxa) are exposed to light [5, 6]suchasin (melanin-based) color of bird specimens [9], and these results 2 International Journal of Zoology Average hue, saturation (a) (c) (e) Average hue, saturation Average hue, saturation Average density (b) (d) (f ) Figure 1: Photographs of the two species studied, golden mouse (a) an d chipmunk (b), and method of measuring color from photographs. Specimens were photographed ((c) and (d)), and image analysis software was used to measure fur color in the selected areas ((e) and (f); see Section 2 for color measurement). eTh agouti, white, and black stripes of chipmunks (f) were measured separately. Rump color (green box in (d)) was also measured in chipmunks. Photo credits: Josh Campbell (a) and Richard Cameron (b). would be helpful for comparison to the melanin-based color have fur that has a golden-brown or tan color throughout of mammals. Doucet and Hill [9] showed how feathers with (Figure 1(a)). The eastern chipmunk has a mixture of agouti melanin-based colors tended to have higher red chroma in and reddish-brown fur, with white and black dorsal stripes older specimens. Since all melanin-based color is formed by (Figure 1(b)). Including chipmunks in this study allowed us a combination of two melanin pigments, eumelanin (which to compare effects of storage on all fur colors (agouti, black, makes dark colors) and pheomelanin (which makes yellow to white, and red). Results of this investigation will bear on all redcolors),theyspeculatedthateumelanin maybemoresus- projects where color of mammal skins is of importance and ceptible to degradation than pheomelanin pigments, which moreover will further enhance understanding of the eeff cts of over time couldleadtoreduced proportionsofthispigment long-term storage on animal tissues. in the feathers, ultimately resulting in higher reflectance at longer wavelengths (i.e., giving the feathers a slightly reddish color). This is in agreement with at least one anecdotal 2. Methods account from a seasoned museum curator who indicated that of the two melanin pigments, eumelanin tends to become 2.1. Museum Specimens. Specimens of each species were paler and redder over time, while pheomelanin becomes paler obtained from the Georgia Museum of Natural History, in with age (personal communication cited in [10]). Athens, GA (USA). While this museum holds specimens Ourprimary objectiveofthe currentstudy wasto from throughout the southeastern United States, we limited determine if the temporal change in color seen in the our analyses here to animals from the State of Georgia, previous red bat study [4] could be seen in other species to minimize the possibility of comparing different races or (with reddish-brown fur) in museum collections. The species animals that may be locally adapted to differing climates. examined were golden mouse (Ochrotomys nuttalli)and east- eTh collection of golden mice from Georgia contained 91 ern chipmunk (Tamias striatus), which both are native to the specimens that had been collected between 1935 and 1996. United States (although we only examined specimens from The eastern chipmunk collection from Georgia consisted of Georgia; see Section 2). As their name suggests, golden mice 49 specimens collected between 1946 and 1996. All had been International Journal of Zoology 3 prepared in a similar manner, that is, as skins placed in a distributed, based on visual inspection of their frequency standardized position (see Figure 1), and with no chemicals distributions. We therefore used General Linear Modeling or preservatives applied to the pelage. All specimens were to determine if pelage color of either species varies through stored in drawers within metal cabinets and were kept as time. For the golden mice, both hue and saturation were used such, as well as in complete darkness, for the entirety of their as dependent variables, gender was a predictor, and body storage life. From the information on the specimen tags, we size (i.e., total length) and collection year were covariates. A recorded the gender and total length of each animal prior to similar approach was used to examine color in chipmunks, photography (later). although here we separately examined each color type, including the agouti, white, and black stripes of the dorsum and the red color of the rump. All analyses were conducted 2.2. Measuring Pelage Color. Regardless of species, each using the Statistica 6.1 software package [ 14]. animal was individually positioned directly under a digital camera on a copystand and photographed (see Figure 1). The same copystand was used for both collections, but at two 3. Results separate times. Golden mice were photographed on January 1, 2011, while chipmunks were photographed on January 17, In the golden mice specimens, there was no significant effect 2013 (although actual dates and times of photography should of body size on pelage hue (𝐹 = 0.951,𝑃 = 0.332 ), nor 1,84 be meaninglessinthisstudy). Allphotography wasdonein was there a difference between males and females ( 𝐹 = 1,84 a room in the museum. In all cases, no camera flash was 0.987, 𝑃 = 0.323 ). There was a nearly significant effect used; artificial lighting was directed toward the specimen of collection year (𝐹 = 3.819,𝑃 = 0.054 ), with more 1,84 from both sides of the camera (using side-mounted lights on recent specimens tending to have larger hue scores (less red; the copystand) so at least within each collection, the lighting Figure 2(a)). eTh analysis of pelage saturation of golden mice for all specimens was standardized. This was important since showed significant variation with body size ( 𝐹 = 16.96, 1,84 we were interested only in the relative dieff rences among 𝑃<0.001 ), no effect of gender ( 𝐹 =1.82,𝑃=0.180 ), and 1,84 individuals within the mice or chipmunk collections, not in a significant relationship with collection year ( 𝐹 =13.43, 1,84 comparing mice versus chipmunk colors. 𝑃 < 0.001 ), such that more recent specimens had lower From the photographs we used image analysis proce- saturation scores (their color was less pure; Figure 2(a)). dures to quantify the degree of redness in the specimens In the analysis of dorsal agouti color in the chipmunks, [4, 11, 12]. For this, images were imported into Adobe there was no effect of body size ( 𝐹 = 0.173,𝑃 = 0.679 ) 1,42 Photoshop with FoveaPro plugins installed (http://www nor of gender (𝐹 = 0.549, 𝑃 = 0.462 )onhue,but 1,42 .reindeergraphics.com/). For the golden mice, an oval selec- a signicfi ant effect of collection year ( 𝐹 =7.71,𝑃= 1,42 tion was drawn over the dorsal surface that covered as much 0.008), with more recent specimens having higher hue scores of the furred area as possible without touching the ears (Figure 2(b)). There was no eeff ct of body size ( 𝐹 =0.087, 1,42 (Figure 1). Using a FoveaPro plugin, the average pixel hue 𝑃 = 0.769 ) or gender (𝐹 = 0.626,𝑃 = 0.433 )onthe 1,42 and saturation values of this selected area were obtained. agouti saturation scores, but a signicfi ant effect of collection With computer software, hue is measured in degrees (0–360), year (𝐹 =7.83,𝑃 = 0.007 ), with more recent specimens 1,42 with lower scores representing redder colors, while brightness having lower saturation scores (Figure 2(b)). Results of the analyses of white and black dorsal stripes on the chipmunks is measured from 0 to 255, with higher scores indicating purer colors. From the chipmunk specimens we first selected showed no eects ff of gender, body size, or collection year, a square region of the dorsal surface that encompassed the on white hue, saturation, or the black density scores (𝑃> stripedregiononthe dorsum (Figure 1), andthenwithinthis 0.1 for all predictor variables in all models). Results of the box we measured color of the agouti, black, and white stripes analyses of hue and saturation of the chipmunk rump color individually.For this,one of us traced theedgeofthe stripes were nearly identical to the analyses of agouti color (i.e., with on the left and right sides, and we obtained the hue and the same signicfi ant predictor variables) and are not reported saturation within these traced areas. For the agouti pelage here. andwhite dorsal stripes, we obtained theaverage hueand In sum, while the magnitude of the effect differed by saturation scores. For the black dorsal stripes, we obtained species, results from analyses of golden mice and chipmunk theaverage pixeldensity scoreofthe traced area,which is a color (at least for the agouti fur) were qualitatively similar; measureof“blackness” andrangesfrom0to 255, with 0being specimens from earlier years tend to be redder than those perfect black and 255 perfect white [13]. These values were from more recent years. This pattern can be visually seen obtained for the left and right sides and averaged for each when photos of representative early and later specimens of specimen. Finally, we also measured the hue and saturation each species are cropped at the region of interest (middle of of the rump of each chipmunk, which we defined as the thedorsum) andplacedside-by-side(Figure 3). region from the base of the tail to where the dorsal stripes end (Figure 1(b)). This region consists of only reddish-brown 4. Discussion fur. Results from this study are consistent with the prior inves- 2.3. Data Analyses. All pelage hue, saturation, and density tigation of red bats from Georgia (from the same museum), values of the golden mice and chipmunks were normally in which older specimens were found to be redder in color 4 International Journal of Zoology r = 0.21, P = 0.048 r = 0.44, P = 0.0017 1930 1940 1950 1960 1970 1980 1990 2000 1940 1950 1960 1970 1980 1990 2000 Collection year Collection year 240 210 r = −0.34, P = 0.0010 r = −0.3, P = 0.0358 205 150 1930 1940 1950 1960 1970 1980 1990 2000 1940 1950 1960 1970 1980 1990 2000 Collection year Collection year (a) Golden mouse (b) Chipmunk (agouti fur only) Figure 2: Relationships between storage time (collection year) and pelage color (hue and saturation) for golden mice (a) and chipmunks (b). Only the values from the agouti pelage of chipmunks are shown. There was no temporal eeff ct on the white and black stripes of chipmunks. than more recent specimens [4]. At the time, it was thought temporal pattern must be common to all three. eTh simplest that this pattern was the result of breakage of hair shaft tips explanation is that the fur of all three species undergoes in older specimens, although further examination of the bat certain biochemical changes in storage, such as breakdown of collection as well as the species considered here found no eumelanin pigment in the hair b fi ers, which was speculated evidence for hair breakage. This can be seen in digital scans by Doucet and Hill [9]. Over time this would result in greater of hair samples (of the agouti fur) taken from early and proportions of the redder pheomelanin pigment in the fur later chipmunk specimens, which show intact guard hairs and a redder overall coat color in older specimens. If this is in both cases (Figure 4). However, these scans also reveal indeed the case, it emphasizes the importance of considering that much of the color variation between older and newer storage time in research studies using mammal skins and specimens is in the fine body hair of the animals, rather than where color is of importance. the thicker guard hairs. In the older specimens, these ne fi eTh re is also the possibility that early collectors may hairs appear redder than in the newer specimens. Meanwhile, have used different methods to prepare study skins at this the thick guard hair appears unchanged. It may be that the museum, which in some cases can cause reddening of pelage thickness and size of the hair determine its susceptibility to [15]. In particular, soaking the skin in tap water to relax it color change. This could also explain why we saw no temporal prior to stuffing appears to cause pelage reddening, and this eeff ctonthe whiteand blackdorsalstripes of thechipmunks, eeff ct can be seen in most mammal species, but especially in which consist primarily of white or black guard hairs (see squirrels [15]. However, whilemostofthe collectors of the Figure 3). earliest specimens (prior to 1960) at the Georgia Museum We therefore have similar results now from three different of NaturalHistory have sincepassed, thereisconsensus mammal species from Georgia, all with distinct life histories, among the current workers that specimens have always been habitat preferences, and so forth. Because of these differences prepared here according to standard mammalogy guidelines in biology and life history, the mechanism behind the [16], which does not include soaking. Less pure Saturation Purer red More red Hue Less red Less pure Saturation Purer red More red Hue Less red International Journal of Zoology 5 1942 1993 (a) (a) 1954 1996 (b) Figure 3: Comparison of representative older and newer specimens (b) of golden mice (a) and chipmunks (b), cropped to show the region measured. Figure 4: Scans of hair samples taken from an older chipmunk specimen and a newer chipmunk specimen, to show differences in color. Hair samples were scanned on a flatbed scanner with no color correction. Samples were cut from the agouti fur on the dorsum of Results from this study lead us to wonder how prevalent the specimens. Note the red coloring of the fine body hair in the older specimen, compared to the newer specimen (white arrows) this phenomenon is in mammalian collections here and in and that there is no breakage of hair tips in the older specimen (black other museums. While our intention here was only to confirm arrows). the existence of the temporal eeff ct found in the prior study of red bats (and we therefore only chose species that had reddish fur, similar to red bats), the lack of color change found in the black and white chipmunk fur suggests that this effect may Barrett contributed helpful comments on the project and on only be observed in species with reddish fur. Moreover, it the biology of golden mice. may be that species with especially fine hairs would also be susceptibletochange(sincethe nfi ebodyhairs of chipmunks changed more than the guard hairs). References A variety of scientific investigations, spanning many [1] P. T. J. Johnson, K. B. Lunde, D. A. Zelmer, and J. K. Werner, decades, have incorporated measures of pelage color of “Limb deformities as an emerging parasitic disease in amphib- museum specimens (e.g., [17–20]). Such studies require that ians: evidence from museum specimens and resurvey data,” all specimens accurately represent their “true” color (i.e., their Conservation Biology,vol.17, no.6,pp. 1724–1737, 2003. color at the time and place of collection). Given this temporal [2] H. B. Shaeff r, R. N. Fisher, and C. Davidson, “The role of natural pattern found here, it would be wise for future investigators history collections in documenting species declines,” Trends in to consider storage time in all analyses of mammalian color, Ecology & Evolution,vol.13, no.1,pp. 27–30, 1998. especially for species with reddish-brown fur. [3] A. C. M. Junqueira, A. C. Lessinger, and A. M. L. Azeredo-Espin, “Methods for the recovery of mitochondrial DNA sequences from museum specimens of myiasis-causing flies,” Medical and Acknowledgments Veterinary Entomology,vol.16, no.1,pp. 39–45, 2002. eTh authors thank Sonia Altizer for use of lab space and [4] A.K.Davis andS.B.Castleberry,“Pelage colorofred bats Liz McGhee for assistance with obtaining specimens. Gary Lasiurus borealis varies with body size: an image analysis of 6 International Journal of Zoology museum specimens,” Current Zoology,vol.56, no.4,pp. 401– 405, 2010. [5] W. B. McKillop, “Induced colour fading in entomological specimens,” J. Waddington and D. M. Rudkin, Eds., pp. 101– 104, Proceedings of the Workshop on Care and Maintenance of Natural History Collections Royal Ontario Museum, Toronto, Canada, 1986. [6] J. Hudon, “Considerations in the conservation of feathers and hair, particularly their pigments,” in Fur Trade Legacy. eTh Preservation of Organic Materials, M. Brunn and J. A. Burns, Eds., pp. 127–147, Canadian Association for Conservation of Cultural Property, Ottawa, Canada, 2005. [7] G. D. McNett and K. Marchetti, “Ultraviolet degradation in carotenoid patches: live versus museum specimens of wood warblers (Parulidae),” Auk,vol.122,no. 3, pp.793–802,2005. [8] J. K. Armenta, P. O. Dunn, and L. A. Whittingham, “Effects of specimen age on plumage color,” Auk,vol.125,no. 4, pp.803– 808, 2008. [9] S.M.Doucet andG.E.Hill,“Do museum specimensaccurately represent wild birds? A case study of carotenoid, melanin, and structural colours in long-tailed manakins Chiroxiphia linearis,” Journal of Avian Biology,vol.40, no.2,pp. 146–156, [10] C. A. Hawks, S. L. Williams, and J. S. Gardner, The Care of Tanned Skins in Mammal Research Collections. Museology,vol. 6, Texas Tech University Publication, 1984. [11] A. K. Davis, “Wing color of monarch butterflies ( Danaus plexippus) in Eastern North America across life stages: migrants are “redder” than breeding and overwintering stages,” Psyche, vol. 2009, Article ID 705780, 5 pages, 2009. [12] A. K. Davis, J. Chi, C. A. Bradley, and S. Altizer, “The redder the better: wing color predicts flight performance in monarch butterflies,” PloS ONE,vol.7,no. 7, ArticleIDe41323, 2012. [13] A.K.Davis,B.D.Farrey, andS.Altizer,“Variationinther- mally induced melanism in monarch butterflies (Lepidoptera: Nymphalidae) from three North American populations,” Jour- nal of eTh rmal Biology , vol. 30, no. 5, pp. 410–421, 2005. [14] Statistica, Statistica Version 6. 1,Statsoft Inc.,2003. [15] S. C. Downing, “Color changes in mammal skins during preparation,” Journal of Mammalogy,vol.26, pp.128–132,1945. [16] A. F. DeBlase and R. E. Martin, “A manual of mammalogy with keys to the families of the world,” in Specimen Preparation and Preservation, chapter 35, Wm. C. Brown Company Publishers, Dubuque, Iowa, USA, 2nd edition, 1981. [17] H. H. Collins, “Studies of the pelage phases and of the nature of color variations in mice of the genus Peromyscus,” Journal of Experimental Zoology,vol.38, pp.45–107, 1923. [18] R. H. Pine,J.E.Rice, J. E. Bucher,D.H.Tank, andA.M. Greenhall, “Labile pigments and u fl orescent pelage in didelphid marsupials,” Mammalia,vol.49, pp.249–256,1985. [19] L. N. Carraway and B. J. Verts, “Geographic variation in pelage color of pino ˜ n mice (Peromyscus truei) in the northern Great Basin and environs,” Western North American Naturalist,vol.62, no. 4, pp. 458–465, 2002. [20] D. Ge,A.A.Lissovsky,L.Xia,C.Cheng,A.T.Smith,and Q. Yang, “Reevaluation of several taxa of Chinese lagomorphs (Mammalia: Lagomorpha) described on the basis of pelage phenotype variation,” Mammalian Biology,vol.77,no.2,pp.113– 123, 2012. 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