TY - JOUR AU1 - Morejohn, G., Victor AU2 - Howard, Walter, E. AB - This paper is an attempt to establish the sequence of molt patterns and the number of annual molts in pocket gophers from Davis (Thomomys bottae navus) and O' Neals (T. b. mewa), California. Investigations were conducted between 1949 and 1955 and were based on laboratory and field studies of more than 600 animals. Histological aspects of hair development are also described herein. Acknowledgements are extended to Jay C. Quast, Nathan W. Cohen, and Henry E. Childs, Jr., for aid in live-trapping and in recording field molt data. Mr. Childs also prepared most of the flat study skins. Seth B. Benson and Robert L. Rudd are gratefully acknowledged for their comments on the study and for reading the manuscript. Methods Live-trapped gophers.— Pocket gophers (T. b. mewa) were periodically live-trapped on a 3.7 acre plot at the San Joaquin Experimental Range, O' Neals, San Joaquin County, California, from 1949 to 1954 (Howard and Childs, MS). Each time an animal was captured, the position of any molt line present (where visible) was recorded on 5 × 8 inch cards containing mimeographed outlines of dorsal and lateral views of a gopher. The pelage color and also the comparative length of hair, if apparent in the two seasonal pelages of molting gophers, were also entered on the card. A total of 789 of these recordings was obtained from 198 individuals. Fourteen gophers living on the plot were dyed as an additional procedure, but this was at a time when trapping was less frequent. Nevertheless, during the ensuing fourteen months, ten of the dyed animals were recaptured a total of 21 times. Kill-trapped gophers.— Flat study skins were prepared from 355 gophers trapped on and around the study plot at the Experimental Range. Only a few skins were obtained from June to September— the season when rangeland gophers show little evidence of surface activity and are difficult to trap. The area of pigmentation on the flesh-side of the skins, indicative of follicular activity, was measured with a planimeter. Similar measurements were also made of the area of each skin that was in summer or winter pelage. The position of molt lines and other data were also obtained from nearly 100 animals collected from irrigated alfalfa fields at Davis. Dyed and bleached gophers.— A technique of dying hair black and of bleaching black hair to light brown was developed by the senior author and D. G. Constantine in 1949 (unpublished). The technique had been employed on studies of molt in cattle and swine, and it was found applicable to other mammalian species as well. To dye the animals, a black human hair dye with an oil base was used. Since it was not water soluble, the dye persisted until the hair was shed. It was diluted with an equal amount of 30-volume (3 %) hydrogen peroxide. Granulated soap was added until a thick liquid was obtained. The soap made application easier, saved dye that would have otherwise run off the gopher, and shortened the time of dye action to 15–20 minutes per animal— half the time otherwise required. Animals were anesthetized with ether, then the dye was applied with a toothbrush. Little dye was applied to the head, for when the animal regained consciousness, it invariably began to clean itself. In so doing, it spread the dye over its head. Application of the dye required approximately five minutes. After the action of the dye was complete, surplus dye was washed off. Excess water was carefully pressed from the hair. The animal was then placed in a container partly filled with cornmeal. Even though each animal attempted to dry itself by pushing through the cornneal, to hasten moisture absorption additional cornmeal was also poured over the drying animal. A similar procedure was followed for the bleach method. Ammonium hydroxide (4 %) was used in place of the dye in a ratio of one part to two parts hydrogen peroxide. The general appearance of bleached gophers was a lighter brown. The bleaching was most effective on the basal portion of the hairs in distinguishing bleached from unbleached hairs. Molt on bleached animals could only be discerned by blowing hair aside in order to check presence of slate-colored basal portions of new hair. The dye method was superior to bleaching. Untreated emerging hair was clearly evident on dyed gophers. The bleach method works better on animals having black pelages. Laboratory procedures,— Four gopher outlines (dorsal, ventral, and two lateral views) were mimeographed on 8½ by 11 inch paper for recording molt progression. Drawings of position of molt lines prior to dying or bleaching were made, and subsequent molt patterns were recorded as often as necessary, usually about every two weeks. All laboratory animals were housed in open-topped, metal-sided cages, with wood shavings as litter. Water was supplied at all times in small dishes or bottles. The bulk of the food consisted of commercial rabbit pellets and rolled oats, but occasionally carrots or potatoes were provided. Temperatures in the laboratory ranged from 16 to 30°C. Molt Patterns Most mammals molt completely, annually or semi-annually. Usually, hair is not shed and regenerated over the entire body surf ace simultaneously, (exceptions are found in young mammals) but begins at one or several places and spreads over the rest of the body. During this process, part of the coat is composed of new hair, and the remainder is composed of old hair. The configurational relationship between old coat areas and new coat areas is referred to as a “molt pattern.” “Molt lines” appear where two seasonal pelages of different color and hair length meet or as a demarcation between two portions of a similar pelage that molted at different times. “Molt” may indicate either an active or a passive process. During the occurrence of follicular activity, an animal is actively molting. In passive molt there is cessation of follicular activity, and no pigmentation is visible on the underside of the skin; yet the animal's coat contains parts of more than one seasonal pelage. Few detailed studies have been made of molt patterns in mammals. Studies of Bassett and Llewellyn (1948),(1949) on silver fox and mink are noteworthy. More recently, Whiteley and Ghadially (1954) studied molt and molt patterns in domestic rabbits by a method of dying hair black. It is of interest that the molt patterns they picture for the domestic rabbit are strikingly similar to those presented in this paper for the pocket gopher. Types of molt patterns in ground squirrels have been demonstrated by Hansen (1954). Cyclical waves of hair regeneration, in which one hair at a time is produced in a follicle, have been demonstrated for the laboratory mouse by Dry (1925)-26) and Wolbach (1951), and the same for the laboratory rat by Haddow et al., (1945), and Durward and Rudall (1949). Hair replacement in these animals usually begins ventrally and gradually spreads dorsally and posteriorly. Molt patterns in deer mice (Storer et al., 1944) resemble those of the laboratory rat and mouse. Nine gophers dyed black and one bleached were observed intensively for a year in the laboratory. At the time of capture all but two of the ten animals possessed one or two molt lines on their backs (Fig. 1, Top). How many of these lines represented active molt and how many passive molt is not known. Only one female (No. 63) continued to molt after being brought into the laboratory, and this molt was on the rump. Other gophers ceased molting in the laboratory for unknown reasons. Nevertheless, all animals started a new molt within four weeks after being dyed. Fig. 1 Open in new tabDownload slide Top: Molt lines of eight pocket gophers (Thomomys bottae navus) represented on one drawing (dorsal view). These eight animals were live-trapped during the period January to April, 1952, and the state of molt was recorded individually. Bottom : Three views of detailed patterns of progression of the second laboratory molt on female pocket gopher no. 63. Successive recordings are numbered 1 to 8 and were taken at intervals of 19, 7, 20, 8, 14, 23, and 20 days, respectively. Molting stopped after region 7 molted. Eleven months after being dyed, the animal was killed. At this time the stippled portion of region 8 was still not molted. Regions of more complex spot-molting around the head and ventral surface are not all numbered in this illustration. Fig. 1 Open in new tabDownload slide Top: Molt lines of eight pocket gophers (Thomomys bottae navus) represented on one drawing (dorsal view). These eight animals were live-trapped during the period January to April, 1952, and the state of molt was recorded individually. Bottom : Three views of detailed patterns of progression of the second laboratory molt on female pocket gopher no. 63. Successive recordings are numbered 1 to 8 and were taken at intervals of 19, 7, 20, 8, 14, 23, and 20 days, respectively. Molting stopped after region 7 molted. Eleven months after being dyed, the animal was killed. At this time the stippled portion of region 8 was still not molted. Regions of more complex spot-molting around the head and ventral surface are not all numbered in this illustration. Fourteen animals living on the study plot were dyed early in February. Gophers there usually begin molting into summer pelage at this time. Two of the 14 had started to molt on the head before they were dyed. One of these was re-trapped 88 days later, when about half molted. The area on the head, which had molted just before being dyed, had not remolted. Eight were recaptured 36 to 42 days later. Some of these individuals had lost as much as 80 per cent of their winter pelage in that time, whereas others had lost less than ten per cent. Several dyed gophers were caught twice between the end of March and May; and during this period little additional molting had occurred, and none of them had molted on the rump No dyed hair was present on one animal caught 10 months later and on two animals trapped 14 months after being dyed. A series of molt pattern progressions in an individual pocket gopher is demonstrated in Figure 1, Bottom. Molt usually started on the feet and head. The tail generally started to molt several days later, but occasionally molt commenced in all three places simultaneously. Sometimes it took place on the nape of the neck or midventral area before beginning on the head or tail. With one individual the tail was the last area to molt. A composite picture of progression of molt was obtained (Fig. 2). However, it should be pointed out that there was much variation in pattern and rate of molt. Figure 2 should be referred to for the following description of molt. Fig. 2 Open in new tabDownload slide Major stages of molt pattern progression in the pocket gopher (Thomomys bottae navus) at Davis. Stippled areas represent hair dyed black; white areas represent new pelage that has replaced dyed hair. See text for details. Fig. 2 Open in new tabDownload slide Major stages of molt pattern progression in the pocket gopher (Thomomys bottae navus) at Davis. Stippled areas represent hair dyed black; white areas represent new pelage that has replaced dyed hair. See text for details. Active molting on the head began with several spots of new hair around the eyes or ears. On the tail it usually began at the tip and progressed toward the body. Molt on the forefeet advanced dorsally to unite with other areas of new hair. Hind and forefeet often molted in narrow bands. This type of molting usually began the toes and progressed toward the elbow. At this stage of molt the overall effect was that of striped legs (Fig. 2, lateral B), but this pattern eventually was lost as areas of new hair fused together. Molt around the eyes and ears expanded over the head in all directions, and molt between the fore legs continued anteriorly along the throat and jaw to the chin. The area around the nose molted and fused with the rest of the new hair of the head. While molting of these areas progressed, spots appeared along the abdomen, and streaks of new hair developed along the mid-line of the ventral side of the body. At this time the forefeet had molted up to the elbows, and a continuous line was often visible running dorsally from the ventral surface of the elbow and anteriorly along the edges of the cheek pouches (cheek pouches were not dyed, thus their molt was not observed). As this line reached a point below the eye it turned dorsally, then posteriorly and progressed below the ear gradually curving dorsally behind the head (Fig. 2, lateral D). The line continued a similar course on the opposite side. On an un-dyed gopher this line can clearly be seen dorsally; however, it cannot be seen in its entirety elsewhere unless the animal is dyed. Along the abdomen the spots and streaks of new hair expanded and fused together. Dorsally the molt line moved posteriorly more rapidly than on the sides. The location of the original molt line along the dorsal surface of dyed gophers (Fig. 1) apparently affected the next molt. Progression of hair replacement posteriorly ceased just short of these lines. Within a few days molt continued from the posterior side of the old molt line leaving unmolted areas of various sizes in front of the original molt line. Eventually these areas also molted. The remaining dyed hair on the gopher at this stage (Fig. 2, dorsal E) was roughly a “lyre-shape” (Applegate and Predmore, 1947) with its ends lying laterally on each side of the head, and the curved part extending laterally along the body and dorsally over the rump. As molt continued, the ends and sides of the “lyre-shape” were gradually broken into irregular spots which later disappeared. Last to molt was the rump and one or two small lateral spots. In general, molt patterns were somewhat similar on all gophers. Six of the ten laboratory animals began a second molt before the first was completed on the rump. They were then redyed. It is of particular interest that the pattern of the second molts showed a striking parallel to the preceding ones in their progression patterns and in manner of molting around the eyes. Also, the regions of the old original molt lines seemed to have the same influence on the time of molt of the adjacent areas. Although the lines were obliterated by the first laboratory molt, the progression of the second molt pattern in this area was similar to the first laboratory molt. This type of molt behavior may also have occurred in field animals, for they also showed molt lines and had irregular molt progression. Frecuency of Molt Pocket gophers from O'Neals display fairly distinct seasonal pelages, the summer coat usually being lighter colored, redder, and often consisting of shorter hairs than the winter coat. This was not clearly evident on some specimens, however. The winter coat was acquired rapidly in the fall, and nearly all gophers had a complete winter coat during December and January (Fig. 3). Females started acquiring a summer pelage sooner than males but did not complete it sooner. Pigmented areas on the flesh-side of skins appeared nearly a month before summer pelage was evident (Fig. 3). After females began molting into a summer pelage, breeding began (February). Following breeding (May) there appeared to be a distinct delay in completion of summer pelage. Kill-trapped pregnant females at this time had considerable pigment on the flesh-side of their skins. It seemed possible that some of them were obtaining part of a second winter coat, but this could not be verified. Dyed gophers retrapped in the field also were slow in obtaining summer pelage, at least during March, April and May. Fig. 3 Open in new tabDownload slide Scatter diagram based on 355 flat skins of the pocket gopher (Thomomys bottae mewa) from O'Neals. Each skin is plotted twice during month captured; once with regard to percentage of summer coat present and once with regard to percentage of pigmented area occurring on the underside of the skin. Follicular activity usually preceded pelage change by approximately one month. Fig. 3 Open in new tabDownload slide Scatter diagram based on 355 flat skins of the pocket gopher (Thomomys bottae mewa) from O'Neals. Each skin is plotted twice during month captured; once with regard to percentage of summer coat present and once with regard to percentage of pigmented area occurring on the underside of the skin. Follicular activity usually preceded pelage change by approximately one month. Few skins were available for the period from May to September. This is the time of year when gophers are less active and difficult to trap. The evidence at hand, however, indicated that a complete summer coat seldom occurred, and, when it did, lasted for only a brief period. New winter pelage frequently began to appear before the summer pelage had replace the previous winter coat on the rump. Bailey (1915) also found winter coats to be acquired more rapidly in the gophers he studied. The frequency of gophers undergoing all stages of molt throughout the year on the study plot is shown in Fig. 4, Top. Fig. 4 Open in new tabDownload slide Top: A comparison is made between skins (Thomomys bottae mewa) of 355 kill-trapped animals and 789 recordings from 198 live-trapped gophers. The percentage of animals that were molting or possessed both a summer and winter coat are plotted by-month. The winter pelage was acquired more rapidly than the summer coat. Bottom: Duration of molting of most of the pelage in pocket gophers (Thomomys bottae navus) from Davis. Vertical lines indicate time of capture, and dashed lines indicate no molting activity. Solid black lines represent the number of days taken to molt the dyed pelage (exclusive of rump region in some), or part of a second molt in progress. Numbers above lines represent approximate days of molting activity. All gophers except ♂ no. 52 were dyed black. Male 52 was bleached, and the actual date of onset of the second molt is only an approximation. Fig. 4 Open in new tabDownload slide Top: A comparison is made between skins (Thomomys bottae mewa) of 355 kill-trapped animals and 789 recordings from 198 live-trapped gophers. The percentage of animals that were molting or possessed both a summer and winter coat are plotted by-month. The winter pelage was acquired more rapidly than the summer coat. Bottom: Duration of molting of most of the pelage in pocket gophers (Thomomys bottae navus) from Davis. Vertical lines indicate time of capture, and dashed lines indicate no molting activity. Solid black lines represent the number of days taken to molt the dyed pelage (exclusive of rump region in some), or part of a second molt in progress. Numbers above lines represent approximate days of molting activity. All gophers except ♂ no. 52 were dyed black. Male 52 was bleached, and the actual date of onset of the second molt is only an approximation. Skins from small juvenile animals, in most cases, showed hair replacement occurring over the entire body simultaneously. The soft, grayish coats also seemed to be replaced more rapidly than adult coats. At O'Neals the first adult pelage was a summer coat. It is possible that with some subadults, an adult winter pelage was acquired on the rump before the juvenile pelage in that region was replaced by a summer coat. Duration of the major part of the molt of laboratory gophers from Davis ranged from 88 to 295 days with an average of 208.7 days per animal (Fig. 4, Bottom). These figures were obtained by considering a molt finished as soon as another one started. With other dyed gophers the rump region retained dyed hair after another molt had begun on the head and feet. Molting of this patch of dyed hair was not consistent. In some individuals the patch was molted soon after beginning of the second molt, but on other occasions the rump patch would not be molted during the second molt; and the old dyed hair would be retained until replaced by a third molt. Two laboratory gophers, a male and a female, retained dyed rump hairs after periods of 17 and 18 months. Five animals retained dyed rump hairs for at least one year. It follows that occasionally the rump region molts only once a year, although the rest of the animal may molt twice a year Such animals, therefore, may possess simultaneously: (1) original dyed hair on rump; (2) a coat produced by the first laboratory molt over the bulk of the body; and (3) new hair on the head, tail or feet replacing (2) above. Although laboratory and field animals, in most cases, possessed no more than two coats at the same time, it was clearly demonstrated with dyed gophers that sometimes there were parts of three coats present. Evidence was found that this manner of molt also appeared in wild gophers. Bailey (1915) mentioned that this manner of molting occurred in high or northern localities in other species of gophers, but he did not determine if the rump region molted once or twice a year. Hair Development Types of hair morphogenesis in mammals have not been adequately studied. The manner of development of single hairs from individual follicles is clear (Butcher, 1951; Noback, 1951), but variations that exist deserve mention. In the chinchilla, hairs emerge from skin pores (follicles) that contain 60–70 individual hairs (Wilcox, 1950). Each hair has its own follicle, and each cluster of hairs consists of one guard hair and many wool hairs. Collectively, the cluster of follicles is called a compound follicle. In general, this type of hair development was found in the pocket gopher. In the gophers studied the total number of hairs in each compound follicle ranged from 8 to 19. Molting and non-molting gopher skin (T. b. navus) was studied microscopically. Pieces of skin were fixed in Bourn's fluid and in Newcomer's fluid (Newcomer, 1953). Serial sections were cut at ten microns and stained with Harris' hematoxylin and eosin. Cross and longitudinal sections were made to reveal the pattern of follicular arrangement and growth (PL I). There was little evidence, in the material examined, of lingering hair germs in the derma or in the stratum subcutaneum. New follicles probably develop from cells at the bases of old hair follicles. As the new follicles begin to develop, growth takes place downward through the derma. Contact with the paniculus carnosus muscle of the skin (PL I, Bottom) may occur with formation of hair within, and elongation, of the follicles. New follicles, lying almost parallel to the surface of the skin, organize into small bundles, and the developing hairs grow upward and emerge through an old compound follicle. Each new hair grows between the old hairs. Old hairs begin to fall out when new hairs are about two thirds grown externally. Counts were made of numbers of compound follicles within an area of skin 5 mm.2 from the region of the mid-back of T. b. mewa. The following figures represent average counts on two animals in each of the following classifications: adult ♂♂ winter pelage, 131 compound follicles; adult ♂♂ summer pelage, 118; adult 9 9 winter pelage, 171; and adult 9 9 summer pelage, 166. Counts were accurately made, but the degree of stretch and shrinkage was probably not the same for each skin. A real difference seems to exist in density of follicles between males and females, but much additional data are needed before conclusions can be drawn. Plate I Open in new tabDownload slide Top: Cross-section of non-molting skin of pocket gopher (Thomomys bottae navus). A complete compound follicle is visible in the dermis consisting of 18 individual hair follicles. Adipose tissue of subcutaneum does not show evidence of inactive hair germs. Tissue was fixed in Bouin's fluid, and serial cross-sections were made at 10 microns. The stain used was Harris' hematoxylin and eosin. Middle: Cross-section of molting skin of pocket gopher (Thomomys botiae navus). No new hairs have erupted through the skin at this stage. Developing follicles can be seen in the subcutaneum, and part of an old compound follicle can be seen in the dermis. Preparation same as above. Bottom: Tangential longitudinal section of actively molting skin of pocket gopher (Thomomys botiae navus). The compound nature of the hair follicles is clearly visible. The hair bulbs, undergoing active mitoses, are seen to extend through the subcutaneum to the paniculus carnosus muscle of the skin. Tissue was fixed in Newcomer's fluid, and serial sections were made at 10 microns. Tissues were stained in Harris' hematoxylin and eosin. Plate I Open in new tabDownload slide Top: Cross-section of non-molting skin of pocket gopher (Thomomys bottae navus). A complete compound follicle is visible in the dermis consisting of 18 individual hair follicles. Adipose tissue of subcutaneum does not show evidence of inactive hair germs. Tissue was fixed in Bouin's fluid, and serial cross-sections were made at 10 microns. The stain used was Harris' hematoxylin and eosin. Middle: Cross-section of molting skin of pocket gopher (Thomomys botiae navus). No new hairs have erupted through the skin at this stage. Developing follicles can be seen in the subcutaneum, and part of an old compound follicle can be seen in the dermis. Preparation same as above. Bottom: Tangential longitudinal section of actively molting skin of pocket gopher (Thomomys botiae navus). The compound nature of the hair follicles is clearly visible. The hair bulbs, undergoing active mitoses, are seen to extend through the subcutaneum to the paniculus carnosus muscle of the skin. Tissue was fixed in Newcomer's fluid, and serial sections were made at 10 microns. Tissues were stained in Harris' hematoxylin and eosin. Discussion Bailey (1915) was the first to describe what he considered to be the typical molt for the genus Thomomys. His description of the molt was based on a large series of conventional round study skins. The conclusions presented herein differ from Bailey's in several major aspects. The points of difference stem primarily from examination of the pigmentation on the flesh-side of gopher skins, prepared as flat skins, and from observations made on living gophers. One or more molt lines observed by Bailey on a gopher skin led him to assume that several “waves” of molt were taking place. If this were true, a gopher replacing its winter coat would have molted as many as five times or more before its full summer pelage was assumed. Material examined in the present study demonstrated that what may appear to be a molt line may indeed be only an area that ceased molting for a time. Since a new coat may appear in an irregular fashion, several molt lines may be present at the same time. In discussing the fall molt, Bailey (op. cit. states that this molt “… seems not to replace the first but to fill up and thicken the coat, while both (coats) may increase in length as the weather becomes more severe.” Five pocket gophers (T. b. navus), which had been dyed previously, were placed in a cold room at 40 degrees Fahrenheit. During a period of approximately five months some molting activity took place, but there was no development that could be attributed to the colder environment. Hair did not grow longer, and old coats did not become denser. It is not known if gophers in a colder climate would behave differently. In describing hair development in the young gopher, Bailey accurately described the first juvenile coat, but due to lack of critical material, he was unable to interpret correctly subsequent molts. Observations based on several skins of very young animals and on captive young (litter mates) of approximately the same age indicate that hair replacement in young gophers is not unlike that of most young mammals studied by other workers. The first coat of fine silky hair is replaced simultaneously over the entire body by a longer silky coat. After acquisition of this coat (complete or incomplete depending on time of year), a juvenile coat begins to make its appearance in the region of the head and progresses over the body in a posterior direction, in a manner similar to that of the adults. Details of exact molt line configurations were not obtained, since young animals were not dyed. The flat skins from O'Neals suggested that subadult pelage on the rump may sometimes molt directly into a winter coat, but at other times all of the subadult pelage was known to have molted into summer pelage before the winter coat appeared. Laboratory evidence of molt patterns in the pocket gopher presented herein need not necessarily be typical for all wild gophers. For a more thorough understanding of molt in wild populations, it is suggested that several dozen field animals be dyed and then retrapped for a year or longer at intervals of about two weeks. Subsequent redying with dyes of different colors should be done before a molt is complete to make sure that certain areas do not molt again before the remainder of the original coat is lost. This information is needed from gophers living at both low and high elevations so that there will be a marked difference in environmental temperatures. Summary Observations of molt were made on more than 600 pocket gophers (Thomomys bottae) from Davis and O'Neals, California. One hundred ninety eight were repeatedly live trapped; nine dyed gophers and one bleached animal were examined periodically in the laboratory; 14 field animals were dyed; 355 flat study skins were analyzed; and nearly 100 other miscellaneous gophers were utilized. The pattern of the progression of molt and the frequency of molt on different parts of the body were established. “Molt lines” sometimes appeared as lines of demarcation between two portions of a similar pelage which molted at different times; in addition, “molt lines” indicated boundaries between summer and winter pelage. Occasionally the rump region skipped a molt. Some animals possessed parts of three coats simultaneously. Rates of follicular activity differ in various parts of the skin. In general, molt patterns of all gophers were similar, but there was a certain degree of variation. Distinctive histological features of hair regeneration in the pocket gopher are described. Literature Cited Applegate V. C. Predmore H. E. 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