Naturwissenschaften 79, 474- 476 (1992) © Springer-Verlag 1992
are small and hardly visible. With increasing day length as well as under experimental photomanipulation [11] the gonads show a high cell proliferation and mature. This phenomenon is well illustrated by the fact that at the end of December testes weigh on the average 0.90 g and are significantly heavier than at the beginning of December (average 0.62 g). From February to July the testosterone-producing tissue weighs 2.51 g and is significantly heavier than from October to December (0.64 g). The annual changes in the testes weight are illustrated in Fig. 1. In adult male ferrets brain weights range from 5.75 to 8.33 g. However, like in the testis, considerable annual changes in the brain weights do occur
Seasonal Changes in Adult Mammalian Brain Weight E. Weiler Institut for Zoologie (Tierphysiologie) der Universit~t, W-7400 TObingen, FRG
In contrast to long-lasting theories claiming that brains possess a minimal capacity for changes in neural morphology and connectivity, we now know that the development of the mammalian brain is not completed at birth [1]. Postnatal changes in the CNS include biochemical [2] and neuronal [3] parameters. Furthermore, postnatal brain development and maturation depend on hormones [4]. This is especially true for brain centers controlling sexual behavior [5]; sex-related morphological differences have been described in the brains of birds [6] and mammals [7]. The idea that there are cyclical anatomical changes in at least some regions of adult brains is rather new and best investigated in the forebrain of songbirds [8]. Such seasonal changes in songbirds can be attributed to sex steroids [6, 9]. Yet, little information is available on seasonal changes in the brains of mammals. To further investigate this phenomenon we used the European ferret (Mustela putorius f. furo L.) a carnivorous mammal which shows typical seasonal breeding activity. Periods of sexual quiescence (fall/winter) alternate with periods of sexual activity (spring/early summer). Over more than one decade a total of 161 adult males (ages 2 0 0 2180 days) were used. Exact birth dates were known for each individual animal. All males were kept under natural light conditions. Data on body weight, testis and brain weights were collected for each month (Table 1). It was ensured that in each month animals 1 year and older were included. From all animals body weight was measured monthly. The brain and testes were removed immediately after the death of the animal and measured with an accuracy of 0.01 g. The body weight of adult male ferrets varies during the course of the year. In fall the average weight increases to about 1300 g and decreases in spring/ summer to less than 1000 g. The reduction in the body weight in spring 474
coincides with a testosterone-induced increase in the metabolic rate [10]. In 99 males the left testis was heavier than the right one; in 26 cases the right testis was heavier. This difference is highly significant with P < 0.001 (sign test). Therefore, as testis weight, the mean between the left and right testis is always given. During the sexually inactive period in autumn/winter, the testes
Table 1. Summarizing results of body, testis and brain weights (g) Month
Average age [days]
Body
Testis
Brain
Number of animals
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
779 472 1187 788 868 1001 433 754 599 1139 1004 628
1327 1281 1122 1111 1085 1067 989 1021 1144 1144 1184 1292
1.67 2.38 2.68 2.67 2.35 2.44 2.31 1.14 1.04 0.65 0.62 0.64
7.19 7.29 7.34 7.39 7.30 7.21 7.28 7.36 6.85 6.80 6.74 6.49
8 8 17 18 25 13 11 14 8 13 13 13
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Fig. 1. Testis weight for each individual animal. During the first half of the year with increasing day length, the testis weight also increases. With decreasing day length the testis weight decreases Naturwissenschaften 79 (1992) © Springer-Verlag 1992
mm
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8"
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Fig. 2. Individual weight of each brain. Brain weights change significantly during the annual cycle. They are higher during spring/summer than during fall/winter 8
I am grateful to Prof. Dr. R. Apfelbach for allowing me to use his data of the years 1979-1984 and for his valuable comments on the manuscript and to an anonymous reviewer.
3
,k ...........A
~
Brain ----,,Ik---Testis -2,5
/
ferrets ontogenetic changes but no seasonal changes in the brain weight could be detected. Already in 1989 Kirn et al. [13] reported that the brain weight of wild male red-winged blackbirds was 8 o70 smaller in the fall than in the spring; yet - in contrast to our finding in the ferret - this difference was greater in females. A drop of 11 °70 in brain weight occurred in laboratoryreared blackbirds kept on short days compared to others kept on long days. In 1991 Nottebohm [8] reported a seasonal reduction of 15 % in some brain nuclei of adult male canaries from spring to fall. It remains to be explored whether the here reported changes in the neural system of the adult male ferret brain represent a system of hormonal dependent plasticity similar to that described for the adult avian brain.
/
/
-2
Received June 9, 1992
7: Q)
% U~
7
1,5
._c
0,5
1'
2
5
4-
5
6
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8
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Fig. 3. Seasonal changes in testis and brain weight (mean values). There seems to be a close correlation between the two curves, with the exception that the brain weight curve follows the testis weight curve with about a 1-month delay (Fig. 2). The data of spring/summer ( J a n u a r y - A u g u s t ) indicate an average brain weight of 7.31 g, while in autumn/winter ( S e p t e m b e r - December) the average brain weight is only 6.73 g (P < 0.001; t-Test). Interestingly, the curve for the brain weight does not parallel the curve for the testis weight directly, but shows roughly a 1-month delay (Fig. 3). Ferrets are considered adult at the age of 150 days. When comparing data of animals younger than 1 year but older than 150 days with those gained from
animals older than 1 year, no age-related differences in the investigated parameters could be detected. Thus, the described annual changes in brain and testis weights are not positively correlated to aging or to changes in the body weight. They rather show a close correlation to seasonal changes in the plasma testosterone level [12]. Yet, it is hard to believe that whole brain volume/weight could change seasonally. However, the dependency of this effect on the testosterone level is further enforced by the fact that so far in female
Naturwissenschaflen 79 (1992) © Springer-Verlag 1992
1. Ebbesson, S. O. E.: Cell Tissue Res. 213, 179 (1980); Kruska, D.: J. Hirnforsch. 28, 59 (1987) 2. Ailing, C., in: Alcohol and the Developing Brain (Rydberg, U., et al., eds.). New York: Raven 1985; Samorajski, T., Rolsten, C., in: Progress in Brain Research, Vol. 40 (Ford, D. H., ed.). Amsterdam-London-New York: Elsevier 1973 3. Meisami, E.: Dev. Brain Res. 46, 9 (1989); Paton, J. A., Nottebohm, F. N.: Science 225, 1046 (1984) 4. Bottjer, S. W., Dignan, T. P. : J. Neurobiol. 19, 624 (1988); Cons, J. M., Timras, P. S.: Environ. Physiol. Biochem. 5, 355 (1975); Dodson, R. E., Shryne, J. E., Gorski, R. A.: J. Comp. Neurol. 275, 623 (1988); Dussault, J. H., Ruel, J." Annu. Rev. Physiol. 49, 321 (1987); Nicholson, J. L., Altman, J.: Science 176, 530 (1972) 5. Meaney, M. J., McEwen, B. S. : Brain Res. 398, 324 (1986) 6. Arnold, A. P., Nottebohm, F., Pfaff, D. W.: J. Comp. Neurol. 165, 487 (1976); Konishi, M., Gurney, M. E." Trends Neurosci. 5, 20 (1982) 7. Arnold, A. P., Breedlove, S. M. : Horm. Behav. 19, 469 (1985); D6hler, K. D., et al., in: Hormones and Behavior in Higher Vertebrates (Balthazart, J., 475
Pr6ve, E., Gilles R., eds.). Berlin-Heidelberg-New York: Springer (1983); Gorski, R. A., Gordon, J. H., Shryne, J. E., Southam, A. M, : Brain Res. 148, 333 (1978) 8. Nottebohm, F.: Science 214, 1368 (1981)
Naturwissenschaften 79, 476-479 (1992)
9. DeVoogd, T. J.: J. Neurobiol. 17, 177 (1986) 10. K/istner, D., Apfelbach, R.: Verh. Dtsch. Zool. Ges. 76, 292 (1983) 11. Mead, R. A., Neirinckx, S.: J. Exp. Zool. 255, 232 (1990); Neal, J., Murphy, B. D., Moger, W. H.,
© Springer-Verlag 1992
Evidence for Lecithotrophic Viviparity in the Living Coelacanth H. Fricke Max-Planck-Institut for Verhaltensphysiologie, W-8130 Seewiesen, F R G J. F r a h m Max-Planck-Institut for Biophysikalische Chemie, W-3400 G0ttingen, F R G The live-bearing coelacanth Latimeria chalumnae has been considered an embryonic cannibal practicing oophagy (ingestion of mature eggs) with a yolk sac placenta for gas exchange and the limited uptake o f maternal nutrients to supplement the e m b r y o ' s yolk reserves [1- 6]. In August 1991 a large female coelcanth (98 kg wet weight, and 179 cm total length) was caught for the first time off Mogambique, western Indian Ocean [7]. The female carried 26 fully developed late-term pups which composed 12.2% of the mother weight (Fig. 1). Their dry weight was on average 23 % below the dry weight of a maturing egg, indicating that embryos
Oliphant, L. W.: Biol. Reproduct. 17, 380 (1977) 12. K~stner, D., Apfelbach, R. : Horm. Res. 25, 178 (1987) 13. Kirn, J., et al." J. Neurobiol. 139, 163 (1989)
tilized eggs ranges between 19 to 59, o f unovulated eggs to maximally 67 [7,12,14,15]. The disproportion between the small number o f late-term pups and high number of ovulated eggs inferred feeding on eggs or egg debris [1,3,6]. Oral ingestion o f excess eggs or of their b r e a k d o w n products was proposed as the main supplementary source of maternal nutrients. The large
depend solely on their own yolk reserves (lecithotrophy). This observation and anatomical findings favor earlier arguments against embryonic cannibalism and m a t r o t r o p h y [8]. Although 172 coelacanth catches have been reported [9], only one gravid female was found among them [10,11]. She carried five advanced pups ( 3 0 1 - 327 m m total length) with welldeveloped yolk sacs ( 7 - 1 2 9 m m in diameter). Thus, the fact that coelacanths are live-bearers was established. Coelacanth eggs ( 8 5 - 9 0 m m diameter, 334 g wet weight, 185 g dry weight [12]) are among the largest in fish; the number of ovulated, unfer-
520 A
50O
E
A 480
'$ 460
Ix• A
[]
A
440 A
420 4OO 300
310
320
330
340
350
360
body size [ m m ]
Fig. 1. Relationship between body size (total length from snouth tip to tip of small supplementary fin) and wet body weight (regression line y = -0.57 x + 480, r e = 0.001). Wet body weight is the weight of the thawed fish taken from the refrigerator; storing temperature 0 to - 4 °C. Symbols of data points indicate the state of yolk sac withdrawl shown in Fig. 2 ( • stage 1 = yolk sac totally withdrawn, zX stage 2 = small slit at ventral site, remnant of external yolk sac with some yolk visible, [] stage 3 = small pouch of an external yolk sac) 476
Fig. 2. Stages of yolk sac withdrawl in lateterm juveniles; a) stage 1, b) stage 2, c) stage 3. Further explanation see Fig. 1
Naturwissenschaften 79 (1992)
© Springer-Verlag 1992
are small and hardly visible. With increasing day length as well as under experimental photomanipulation [11] the gonads show a high cell proliferation and mature. This phenomenon is well illustrated by the fact that at the end of December testes weigh on the average 0.90 g and are significantly heavier than at the beginning of December (average 0.62 g). From February to July the testosterone-producing tissue weighs 2.51 g and is significantly heavier than from October to December (0.64 g). The annual changes in the testes weight are illustrated in Fig. 1. In adult male ferrets brain weights range from 5.75 to 8.33 g. However, like in the testis, considerable annual changes in the brain weights do occur
Seasonal Changes in Adult Mammalian Brain Weight E. Weiler Institut for Zoologie (Tierphysiologie) der Universit~t, W-7400 TObingen, FRG
In contrast to long-lasting theories claiming that brains possess a minimal capacity for changes in neural morphology and connectivity, we now know that the development of the mammalian brain is not completed at birth [1]. Postnatal changes in the CNS include biochemical [2] and neuronal [3] parameters. Furthermore, postnatal brain development and maturation depend on hormones [4]. This is especially true for brain centers controlling sexual behavior [5]; sex-related morphological differences have been described in the brains of birds [6] and mammals [7]. The idea that there are cyclical anatomical changes in at least some regions of adult brains is rather new and best investigated in the forebrain of songbirds [8]. Such seasonal changes in songbirds can be attributed to sex steroids [6, 9]. Yet, little information is available on seasonal changes in the brains of mammals. To further investigate this phenomenon we used the European ferret (Mustela putorius f. furo L.) a carnivorous mammal which shows typical seasonal breeding activity. Periods of sexual quiescence (fall/winter) alternate with periods of sexual activity (spring/early summer). Over more than one decade a total of 161 adult males (ages 2 0 0 2180 days) were used. Exact birth dates were known for each individual animal. All males were kept under natural light conditions. Data on body weight, testis and brain weights were collected for each month (Table 1). It was ensured that in each month animals 1 year and older were included. From all animals body weight was measured monthly. The brain and testes were removed immediately after the death of the animal and measured with an accuracy of 0.01 g. The body weight of adult male ferrets varies during the course of the year. In fall the average weight increases to about 1300 g and decreases in spring/ summer to less than 1000 g. The reduction in the body weight in spring 474
coincides with a testosterone-induced increase in the metabolic rate [10]. In 99 males the left testis was heavier than the right one; in 26 cases the right testis was heavier. This difference is highly significant with P < 0.001 (sign test). Therefore, as testis weight, the mean between the left and right testis is always given. During the sexually inactive period in autumn/winter, the testes
Table 1. Summarizing results of body, testis and brain weights (g) Month
Average age [days]
Body
Testis
Brain
Number of animals
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
779 472 1187 788 868 1001 433 754 599 1139 1004 628
1327 1281 1122 1111 1085 1067 989 1021 1144 1144 1184 1292
1.67 2.38 2.68 2.67 2.35 2.44 2.31 1.14 1.04 0.65 0.62 0.64
7.19 7.29 7.34 7.39 7.30 7.21 7.28 7.36 6.85 6.80 6.74 6.49
8 8 17 18 25 13 11 14 8 13 13 13
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!
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4
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6
7 Month
8
9
I'0 1'1
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Fig. 1. Testis weight for each individual animal. During the first half of the year with increasing day length, the testis weight also increases. With decreasing day length the testis weight decreases Naturwissenschaften 79 (1992) © Springer-Verlag 1992
mm
m
8"
g
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Fig. 2. Individual weight of each brain. Brain weights change significantly during the annual cycle. They are higher during spring/summer than during fall/winter 8
I am grateful to Prof. Dr. R. Apfelbach for allowing me to use his data of the years 1979-1984 and for his valuable comments on the manuscript and to an anonymous reviewer.
3
,k ...........A
~
Brain ----,,Ik---Testis -2,5
/
ferrets ontogenetic changes but no seasonal changes in the brain weight could be detected. Already in 1989 Kirn et al. [13] reported that the brain weight of wild male red-winged blackbirds was 8 o70 smaller in the fall than in the spring; yet - in contrast to our finding in the ferret - this difference was greater in females. A drop of 11 °70 in brain weight occurred in laboratoryreared blackbirds kept on short days compared to others kept on long days. In 1991 Nottebohm [8] reported a seasonal reduction of 15 % in some brain nuclei of adult male canaries from spring to fall. It remains to be explored whether the here reported changes in the neural system of the adult male ferret brain represent a system of hormonal dependent plasticity similar to that described for the adult avian brain.
/
/
-2
Received June 9, 1992
7: Q)
% U~
7
1,5
._c
0,5
1'
2
5
4-
5
6
7 Month
8
9
1'0
1'1
1~2
Fig. 3. Seasonal changes in testis and brain weight (mean values). There seems to be a close correlation between the two curves, with the exception that the brain weight curve follows the testis weight curve with about a 1-month delay (Fig. 2). The data of spring/summer ( J a n u a r y - A u g u s t ) indicate an average brain weight of 7.31 g, while in autumn/winter ( S e p t e m b e r - December) the average brain weight is only 6.73 g (P < 0.001; t-Test). Interestingly, the curve for the brain weight does not parallel the curve for the testis weight directly, but shows roughly a 1-month delay (Fig. 3). Ferrets are considered adult at the age of 150 days. When comparing data of animals younger than 1 year but older than 150 days with those gained from
animals older than 1 year, no age-related differences in the investigated parameters could be detected. Thus, the described annual changes in brain and testis weights are not positively correlated to aging or to changes in the body weight. They rather show a close correlation to seasonal changes in the plasma testosterone level [12]. Yet, it is hard to believe that whole brain volume/weight could change seasonally. However, the dependency of this effect on the testosterone level is further enforced by the fact that so far in female
Naturwissenschaflen 79 (1992) © Springer-Verlag 1992
1. Ebbesson, S. O. E.: Cell Tissue Res. 213, 179 (1980); Kruska, D.: J. Hirnforsch. 28, 59 (1987) 2. Ailing, C., in: Alcohol and the Developing Brain (Rydberg, U., et al., eds.). New York: Raven 1985; Samorajski, T., Rolsten, C., in: Progress in Brain Research, Vol. 40 (Ford, D. H., ed.). Amsterdam-London-New York: Elsevier 1973 3. Meisami, E.: Dev. Brain Res. 46, 9 (1989); Paton, J. A., Nottebohm, F. N.: Science 225, 1046 (1984) 4. Bottjer, S. W., Dignan, T. P. : J. Neurobiol. 19, 624 (1988); Cons, J. M., Timras, P. S.: Environ. Physiol. Biochem. 5, 355 (1975); Dodson, R. E., Shryne, J. E., Gorski, R. A.: J. Comp. Neurol. 275, 623 (1988); Dussault, J. H., Ruel, J." Annu. Rev. Physiol. 49, 321 (1987); Nicholson, J. L., Altman, J.: Science 176, 530 (1972) 5. Meaney, M. J., McEwen, B. S. : Brain Res. 398, 324 (1986) 6. Arnold, A. P., Nottebohm, F., Pfaff, D. W.: J. Comp. Neurol. 165, 487 (1976); Konishi, M., Gurney, M. E." Trends Neurosci. 5, 20 (1982) 7. Arnold, A. P., Breedlove, S. M. : Horm. Behav. 19, 469 (1985); D6hler, K. D., et al., in: Hormones and Behavior in Higher Vertebrates (Balthazart, J., 475
Pr6ve, E., Gilles R., eds.). Berlin-Heidelberg-New York: Springer (1983); Gorski, R. A., Gordon, J. H., Shryne, J. E., Southam, A. M, : Brain Res. 148, 333 (1978) 8. Nottebohm, F.: Science 214, 1368 (1981)
Naturwissenschaften 79, 476-479 (1992)
9. DeVoogd, T. J.: J. Neurobiol. 17, 177 (1986) 10. K/istner, D., Apfelbach, R.: Verh. Dtsch. Zool. Ges. 76, 292 (1983) 11. Mead, R. A., Neirinckx, S.: J. Exp. Zool. 255, 232 (1990); Neal, J., Murphy, B. D., Moger, W. H.,
© Springer-Verlag 1992
Evidence for Lecithotrophic Viviparity in the Living Coelacanth H. Fricke Max-Planck-Institut for Verhaltensphysiologie, W-8130 Seewiesen, F R G J. F r a h m Max-Planck-Institut for Biophysikalische Chemie, W-3400 G0ttingen, F R G The live-bearing coelacanth Latimeria chalumnae has been considered an embryonic cannibal practicing oophagy (ingestion of mature eggs) with a yolk sac placenta for gas exchange and the limited uptake o f maternal nutrients to supplement the e m b r y o ' s yolk reserves [1- 6]. In August 1991 a large female coelcanth (98 kg wet weight, and 179 cm total length) was caught for the first time off Mogambique, western Indian Ocean [7]. The female carried 26 fully developed late-term pups which composed 12.2% of the mother weight (Fig. 1). Their dry weight was on average 23 % below the dry weight of a maturing egg, indicating that embryos
Oliphant, L. W.: Biol. Reproduct. 17, 380 (1977) 12. K~stner, D., Apfelbach, R. : Horm. Res. 25, 178 (1987) 13. Kirn, J., et al." J. Neurobiol. 139, 163 (1989)
tilized eggs ranges between 19 to 59, o f unovulated eggs to maximally 67 [7,12,14,15]. The disproportion between the small number o f late-term pups and high number of ovulated eggs inferred feeding on eggs or egg debris [1,3,6]. Oral ingestion o f excess eggs or of their b r e a k d o w n products was proposed as the main supplementary source of maternal nutrients. The large
depend solely on their own yolk reserves (lecithotrophy). This observation and anatomical findings favor earlier arguments against embryonic cannibalism and m a t r o t r o p h y [8]. Although 172 coelacanth catches have been reported [9], only one gravid female was found among them [10,11]. She carried five advanced pups ( 3 0 1 - 327 m m total length) with welldeveloped yolk sacs ( 7 - 1 2 9 m m in diameter). Thus, the fact that coelacanths are live-bearers was established. Coelacanth eggs ( 8 5 - 9 0 m m diameter, 334 g wet weight, 185 g dry weight [12]) are among the largest in fish; the number of ovulated, unfer-
520 A
50O
E
A 480
'$ 460
Ix• A
[]
A
440 A
420 4OO 300
310
320
330
340
350
360
body size [ m m ]
Fig. 1. Relationship between body size (total length from snouth tip to tip of small supplementary fin) and wet body weight (regression line y = -0.57 x + 480, r e = 0.001). Wet body weight is the weight of the thawed fish taken from the refrigerator; storing temperature 0 to - 4 °C. Symbols of data points indicate the state of yolk sac withdrawl shown in Fig. 2 ( • stage 1 = yolk sac totally withdrawn, zX stage 2 = small slit at ventral site, remnant of external yolk sac with some yolk visible, [] stage 3 = small pouch of an external yolk sac) 476
Fig. 2. Stages of yolk sac withdrawl in lateterm juveniles; a) stage 1, b) stage 2, c) stage 3. Further explanation see Fig. 1
Naturwissenschaften 79 (1992)
© Springer-Verlag 1992
