Vol. 275, Issue 6, R2012-R2022, December 1998
Photoperiodic responses of four wild-trapped desert rodent
species
Hanan A.
El-Bakry1,2,
Wafaa M.
Zahran1, and
Timothy J.
Bartness2,3
1 Department of Zoology, Minia
University, 61111 Minia, Egypt, and Departments of
2 Biology and
3 Psychology, Georgia State
University, Atlanta, Georgia 30303
 |
ABSTRACT |
The purpose of this study was to examine
the effect of the photoperiod on reproductive status and body and lipid
masses in four Egyptian desert rodent species
(Dipodillus dasyurus,
Acomys cahirinus,
Gerbillus andersoni, and
Gerbillus pyramidum). Adult males
and females were housed in long days for 11 wk. At that time, one-half
of the animals were killed and the remaining animals were moved to
short days (SDs) for 11 wk. Some individuals of Gerbillus andersoni and
Gerbillus pyramidum had access to
running wheels. Testes index and spermatogenesis, but not testis mass, were decreased in all species in SDs. In contrast, SDs did not affect
female reproductive status in all species. Exercise stimulated spermatogenesis but did not affect female reproductive status. SDs
increased body and lipid masses in male
Acomys
cahirinus, but not in other species.
Collectively, these desert rodent species were responsive to day length
changes, but these changes alone did not induce robust alterations in
reproductive status and body and lipid masses.
white adipose tissue; gerbils; mice; reproduction; body weight; exercise
| |
INTRODUCTION |
SEASONAL CHANGES in the environment can affect a wide
range of physiological and behavioral processes in most nontropical mammalian species. For example, dramatic changes in reproductive activity occur across the seasons. Food availability, rainfall, temperature, and day length (i.e., photoperiod) are among the environmental factors that affect the time of onset and the duration of
the reproductive season (31). The annual change in day length, however,
is the principal environmental cue controlling the timing of
reproduction for many nontropical mammals (9,15); other environmental factors serve to shape breeding seasons more subtly. A variety of other
seasonal physiological responses often accompany the photoperiod-induced alterations in reproductive status and include changes in pelage (14), body fat (4), and thermogenesis (22). These
seasonal responses also are typically regulated by changes in the
photoperiod (3).
Seasonal variations in reproductive activity also occur in desert
rodents (11, 28, 29, 40, 41, 47). Nevertheless, very little is known
about the role of the photoperiod in the control of reproduction or
other seasonal responses in desert rodents. The present study addressed
the photoresponsiveness of four Egyptian desert rodent species:
Wagner's Dipodils (Dipodillus dasyurus), spiny mice
(Acomys
cahirinus), Anderson's gerbils
(Gerbillus andersoni), and greater
gerbils (Gerbillus pyramidum).
Limited field data indicate the presence of seasonal reproductive
cycles in these species (23, 35). Specifically,
Acomys
cahirinus breeds throughout most of the
year (February to October), whereas the other three species breed from
fall to late spring with a summer hiatus in reproduction (23). The
presence of winter breeding in these animals could be due to one of
several possibilities. First, these animals could be short day (SD)
breeders, such that reproduction is facilitated by SDs and inhibited by
long days (LDs). Second, they may have a photoperiodic system much like that of typical LD breeding rodents, but the potential inhibitory effect of SDs is overridden by other environmental factors such as
ambient temperature, rainfall, humidity, or food availability. Third,
these animals may be reproductively nonresponsive to the photoperiod
and instead use other predictors to time their reproduction. Fourth,
seasonality in these animals may be a consequence of an opportunistic
strategy in which reproduction is restricted to the times when climatic
and nutritional conditions are optimal without the use of any
environmental predictors. In terms of the last possibility,
reproduction in these desert species might occur in SDs when ambient
temperatures tend to be mild, rainfall more likely, and food generally
more abundant than in the LDs of summer. The purpose of the present
experiment was to examine the role of the photoperiod in the control of
reproductive status and body and lipid masses in four desert
species. Because the availability of running wheels can
stimulate the hypothalamic-gonadal axis (27, 38) and interact with the
photoperiod (6, 16, 39), we also tested the effects of exercise on
reproductive status in LD- and SD-housed animals.
| |
MATERIALS AND METHODS |
Animals
Adult wild-trapped males and females of four rodent species
[Dipodillus dasyurus
(n = 22),
Acomys
cahirinus
(n = 21), Gerbillus andersoni (n = 36),
Gerbillus pyramidum
(n = 35)] were obtained from a
commercial supplier (El-Hakim) in August 1996. On arrival, the animals
of each species were divided on the basis of gender and group housed
(7-10 per cage). They were maintained for 6 wk in LDs
("summerlike"; 14-10-h light-dark cycle; lights on at 0300, lights off at 1700) at a constant temperature (22 ± 2°C) before the start of the experiment. This LD photoperiod was chosen because it
represented the longest day length that occurs at the latitude where
the animals live (30°N; Ref. 5). Food (Purina Rodent Chow 5001) and
tap water were available ad libitum throughout the experiment. All
experimental procedures were approved by the Georgia State University
Institutional Animal Care and Use Committee, Public Health Services
guidelines and also were in accordance with Centers for Disease Control
guidelines for housing and handling wild animals (biosafety level 2).
Experimental Design
Experiment
1. All individuals of
Dipodillus dasyurus and
Acomys cahirinus were weighed and
singly housed in polypropylene cages, each equipped with a running
wheel. Locomotor activity was monitored for 11 wk, and body mass was
measured weekly to the nearest 0.01 g. After this time,
one-half of the animals were anesthetized with methoxyflurane vapors
(Metofane, Pitman-Moore, Mundelein, IL) and killed by decapitation,
their tissues were harvested, reproductive status was assessed, and
carcass composition was measured. The remaining animals were
transferred to SDs ("winterlike"; 10:14-h light-dark; lights on
at 0600). The length of the SDs represented the shortest day length at
the latitude in which the animals were trapped (5). Body mass was
measured weekly to the nearest 0.01 g. Eleven weeks later the animals
were killed and their tissues were removed and processed as above for
the LD-housed animals.
Experiment 2.
Experiment
2 was designed to test whether
exercise affects the reproductive status of LD- or SD-housed animals. Because only a few individuals of Dipodillus
dasyurus and Acomys cahirinus survived trapping and shipping, these two
species were not included in this experiment. Individuals of
Gerbillus andersoni and
Gerbillus pyramidum were singly housed
and divided into two groups balanced for body mass. Animals of the
first group were given access to running wheels, whereas the others
served as sedentary controls. The same protocol described above for the
other two species was followed, except that before being transferred to SDs the males were anesthetized with methoxyflurane and the length and
width of the right testis were measured externally through the scrotal
skin using handheld calipers. Testicular length and width also were
recorded for the males killed in both LDs and SDs. The testicular index
was calculated for each animal by multiplying the testis length by
testis width. This was not done for the other two species
(Dipodillus dasyurus and
Acomys cahirinus) because their
testes are located intra-abdominally. Although there was a possibility
that these animals were reproductively immature, this was unlikely
because several females were pregnant by the time of their arrival.
Tissue Masses
Various white adipose tissue (WAT) pads, including the inguinal WAT
(IWAT), retroperitoneal WAT (RWAT), epididimal WAT (in males), and
parametrial WAT (in females) pads were harvested, blotted dry, weighed,
and replaced in the carcass.
Reproductive Status
In all groups, male and female reproductive status was assessed by
determining the paired testes or uterine masses, respectively. In
addition, testicular indexes were calculated in two species (Gerbillus andersoni and
Gerbillus pyramidum) as above. The
testes and ovaries of both species were stored in Bouin's fixative for histological examination of reproductive status (see
Histological Analysis of the
Gonads).
Carcass Composition
Carcass composition was measured using a modification (2) of the method
of Leshner et al. (30). Briefly, the shaved eviscerated carcass was
weighed to determine carcass wet weight and dried at 80-85°C
to a constant weight to assess carcass water. The dehydrated carcass
was blended, lipid was extracted with the use of petroleum ether, and
the lipid content was determined gravimetrically. The remaining
dehydrated delipidated tissue was termed fat-free dry mass (FFDM).
Histological Analysis of the Gonads
Males. Testes were fixed in Bouin's
solution for 2 days, dehydrated, embedded in paraplast,
sectioned at 6 µm, and stained with hematoxylin and eosin. The
functional state of the testes was determined using the criteria of
Grocock and Clarke (18) with some modifications due to the
heterogeneity of the testis sections. A spermatogenic index with values
0-5 was applied to 100 randomly selected seminiferous tubules,
where 5 is large seminiferous tubules with complete spermatogenesis; 4 is complete spermatogenesis but the number of elongated spermatids and
spermatozoa were reduced; 3 is the number of spermatozoa and elongated
spermatids further decreased; 2 is only round spermatids found with no
elongated spermatids; 1 is only Sertoli cells, spermatogonia, and
primary spermatocytes found; 0 is only Sertoli cells present.
Females. The ovaries were stored in
Bouin's fixative for 24 h, dehydrated, and embedded in paraplast.
Serial sections with a thickness of 6 µm were cut and stained with
hematoxylin and eosin. The functional state of the ovaries was assessed
by examining the number of follicles and corpora lutea in all serial
sections throughout one ovary of each animal (36).
Statistical Analysis
Body mass and spermatogenic index were analyzed with mixed models ANOVA
(NCSS 97, NCSS statistical software). Post hoc comparisons of pair-wise
means were made using Duncan's multiple-range tests when appropriate.
WAT pad, testes and uterine masses, testes indexes, and carcass
components were analyzed with a between-subject ANOVA (Systat version
6.0, SPSS). Tukey's honestly significant difference tests were used as
post hoc tests when appropriate. Differences between group means were
considered statistically significant if
P < 0.05. Test values and exact
probabilities are not shown for clarity and simplicity of presentation
of the findings.
| |
RESULTS |
Body Mass
Males had greater body masses than females in
Dipodillus dasyurus,
Gerbillus andersoni, and
Gerbillus pyramidum throughout the
study, but this only was statistically significant for
Gerbillus pyramidum
(P < 0.05;
Figs.
1A and
2). Female
Acomys
cahirinus were heavier than males in
all experimental conditions, but these differences were not
statistically significant (Fig. 1B).
Both LD- and SD-housed Acomys
cahirinus and
Gerbillus pyramidum significantly increased their body masses across the experiment
(P < 0.05; Figs. 1B and
2B) but were not significantly
different from one another. There was no difference in body mass
between LD- and SD-housed Dipodillus
dasyurus (Fig.
1A). There was a significant
initial decline in body mass in the first week of LD exposure in
Gerbillus andersoni
(P < 0.05; Fig.
2A) that never recovered fully. Body mass was not affected by photoperiod, exercise, or their interaction in
Gerbillus andersoni or
Gerbillus pyramidum (Fig. 2).
View larger version (19K):
[in this window]
[in a new window]
|
Fig. 1.
Mean ± SE body mass for male and female Dipodillus
dasyurus (A) and
Acomys cahirinus
(B). SD, short photoperiod.
|
|
View larger version (26K):
[in this window]
[in a new window]
|
Fig. 2.
Mean ± SE body mass for male and female Gerbillus
andersoni (A) and
Gerbillus pyramidum
(B). Sedentary, animals housed in
conventional cages; Exercising, animals given access to running
wheels.
|
|
Fat Pad Masses
IWAT and RWAT masses were increased in male Gerbillus
pyramidum compared with both LD- and SD-housed females
(P < 0.05; Table 1). Fat pad masses were not different
between LD- and SD-housed animals of all species studied except for two
exceptions. First, the IWAT mass of SD-housed male
Acomys
cahirinus was greater than that of
their LD-housed counterparts (P < 0.05; Table 1). Second, the photoperiod, combined with the access to an
exercise wheel, resulted in greater IWAT mass in SD- than LD-housed
Gerbillus andersoni
(P < 0.05; Table 1).
Carcass Composition
Two gender effects were found among these species for the carcass
composition measures. First, all carcass components were greater in
male Gerbillus pyramidum than females
in both photoperiods for absolute (P < 0.05; Table 2), but not relative
(corrected for body masses), measures. Second, carcass lipid content
was greater in female Acomys
cahirinus than in males in both
photoperiods (P < 0.05; Table 2). SD
exposure increased absolute and relative carcass lipid content in male
Acomys
cahirinus
(P < 0.05; Table 2). Finally,
exercise did not affect carcass composition, except for lipid and FFDM
responses in SD-housed Gerbillus
andersoni. Specifically, lipid content increased and
FFDM decreased in SD-housed wheel running animals compared with their
sedentary counterparts (P < 0.05;
Table 2).
Reproductive Status
Males. Neither absolute nor relative
testes masses differed significantly between LD- and SD-housed males of
any species (Table 3). The testes of both
LD- and SD-housed Dipodillus dasyurus had very low numbers of seminiferous tubules (i.e., <100). Therefore, this species was excluded from further statistical analysis of spermatogenic activity, although the testicular tissues of all animals
were examined histologically and the same criteria for judging the
spermatogenic activity in all other species were followed. Testes of
LD-housed male Acomys
cahirinus and
Dipodillus dasyurus were active
spermatogenically, and the majority of the seminiferous tubules were in
complete spermatogenesis with large numbers of spermatozoa in their
lumens (index 5; Figs.
3A and
4A).
Eleven weeks of SD exposure caused a pronounced decrease in the
spermatogenic activity, but none of the males underwent complete
gonadal regression. Specifically, the number of seminiferous tubules
with spermatogenic index of 5 significantly decreased, whereas the
number of seminiferous tubules with spermatogenic index of 4, 3, 2, and
1 significantly increased (P < 0.05;
Figs. 3A and
4B).
View larger version (14K):
[in this window]
[in a new window]
|
Fig. 3.
Spermatogenic index of male Acomys
cahirinus (A),
Gerbillus pyramidum
(B), and Gerbillus
andersoni (C). LD,
long photoperiod; LDWR, LD-housed wheel running animals; SDWR,
SD-housed wheel running animals; LDSED, LD-housed sedentary animals;
SDSED, SD-housed sedentary animals.
* P < 0.05 vs. LD-housed
animals;
a P < 0.05 vs. LD-housed wheel running animals;
b P < 0.05 vs. LD-housed sedentary animals. See
MATERIALS AND METHODS for details.
|
|
View larger version (157K):
[in this window]
[in a new window]
|
Fig. 4.
Testis sections of Dipodillus
daysurus. Spermatogenically active
testes from LD-housed animal (A) and
SD-housed animal (B); all stages of
spermatogenesis are present with the tails of mature spermatozoa
extending into the lumen of the seminiferous tubule (L). Note reduced
spermatogenesis in SD-housed animal. Bar, 50 µm.
|
|
Neither exercise nor photoperiod affected absolute or relative testes
masses in Gerbillus pyramidum and
Gerbillus andersoni (Table 3). In
contrast, photoperiod, but not exercise, significantly affected
testicular index (Table 4). Specifically,
testicular indexes were significantly lower in SD- compared with
LD-housed animals (P < 0.05; Table
4). These results also were found when comparing testicular indexes for
the same animals before and after transferring them to SDs (Table 4).
Photoperiod and exercise conditions did not interact to affect the
testicular indexes in any species.
Spermatogenic activity in the seminiferous tubules was markedly
decreased in SD-housed Gerbillus
pyramidum and Gerbillus
andersoni compared with LD-housed animals
(P < 0.05; Fig. 3,
B and
C). In addition, there was a
significant effect of exercise on spermatogenic activity. Specifically,
sedentary animals exhibited less spermatogenic activity compared with
wheel running animals in that sedentary animals had a significantly
decreased number of seminiferous tubules with spermatogenic index of 5 and an increased number of seminiferous tubules with spermatogenic
index of 4, 3, 2, and 0 (Fig. 3, B and
C). Photoperiod and exercise also
did not interact to affect spermatogenic activity in any species. There
was a clear difference in the response of these two Gerbillus
species to SD exposure. That is, SD-housed Gerbillus
andersoni had two distinct testicular responses. First,
spermatogenic activity was less than that of the LD-housed animals, but
the difference was moderate despite being statistically significant.
Specifically, the seminiferous tubules had all stages of
spermatogenesis, but the number of spermatozoa and elongated spermatids
dramatically decreased (Fig. 5, A and B). Second, spermatogenesis was
inhibited to a great extent associated with a pronounced testicular
regression. Specifically, spermatogenesis was arrested at the early
stages with absence of spermatozoa as well as elongated and round
spermatids and presence of necrotic cells in many of the seminiferous
tubules (Fig.
5C). The
diameter of the seminiferous tubules also was greatly reduced (Fig.
5C). The latter pattern was found in
sedentary animals and was seen in 25% of exercising
Gerbillus andersoni. In contrast,
although male Gerbillus pyramidum had
moderate, but significant, changes in spermatogenic activity in which
the number of spermatozoa and spermatids greatly decreased in SDs,
there was no evidence of complete testicular regression (Fig.
6, A and
B).
View larger version (104K):
[in this window]
[in a new window]
|
Fig. 5.
Testis sections of Gerbillus andersoni
from LD-housed animal (A),
illustrating full spermatogenic activity with the tails of mature
spermatozoa extending into the lumen of the seminiferous tubule and
from SD-housed wheel running animal (B), showing less
spermatogenic activity. Note that some seminiferous tubules still have
maturing spermatozoa (arrow). C is
from SD-housed sedentary animal, showing severe testicular regression.
Note absence of late stages of spermatogenesis (long spermatids and
spermatozoa), presence of many necrotic cells (arrow), and the reduced
diameter of the seminiferous tubules. All sections are at the same
magnification. Bar, 50 µm.
|
|
View larger version (148K):
[in this window]
[in a new window]
|
Fig. 6.
Testis sections of Gerbillus
pyramidum. Spermatogenically active testis are from
sedentary LD-housed animal (A),
illustrating full spermatogenic activity and from from SD-housed
sedentary animal (B), showing
reduced spermatogenesis. Bar, 50 µm.
|
|
Females. Photoperiod did not affect
the female reproductive status of any of the species. That is, uterine
masses did not differ significantly between LD- and SD-exposed animals
(Table 3). Exercise by itself, or in conjunction with SD exposure, also did not influence the uterine masses (Table 3). These results were
confirmed by the histological examination of the ovaries. Specifically,
females of all species had all stages of folliculogenesis in both LDs
and SDs (data not shown).
| |
DISCUSSION |
On the basis of the limited field data available for these and related
desert species, we predicted that short photoperiods would stimulate
and long photoperiods would inhibit reproductive status; however, this
hypothesis was not supported. Changes in the photoperiod affected
reproductive status only in males of the four desert rodent species
studied (i.e., Acomys
cahirinus, Dipodillus
dasyurus, Gerbillus
pyramidum, and Gerbillus
andersoni), albeit somewhat subtly and then opposite
to what we predicted. That is, SD exposure decreased testes index and
spermatogenesis (as indicated by a reduced spermatic index) but did not
affect testes wet masses. The photoperiod did not affect reproductive status for females in any of the species. Specifically, the ovaries of
all species had complete ovarian folliculogenesis in both photoperiods. Exercise stimulated spermatogenesis, but not testes masses or indexes
in both gerbil species compared with their sedentary counterparts and
did not affect female reproductive status. Finally, the photoperiod minimally affected body and fat pad masses and carcass composition, except for male Acomys
cahirinus, where IWAT mass and carcass lipid content were increased after SD exposure.
The results of the present study are consistent with studies on the
effects of the photoperiod on desert pocket mice
(Perognathus formosus). In this
species, LDs stimulate or maintain reproductive functions. The effect
of SDs, however, depends on the environmental conditions (e.g.,
temperature, humidity) that precede them (24). SDs also do not affect
body and epipidimal fat pad masses in this species (24).
Reproduction in the field is seasonal in the desert rodent species
studied in the present experiments, with winter breeding and summer
reproductive quiescence (23, 35). Because the animals used in the
present experiments were trapped during lengthening days and held in
LDs in the laboratory, it is possible that they became photorefractory
to the presumed inhibitory effects of LD exposure. Reproductive status
was, however, decreased in males of all species after SD exposure; thus
it seems unlikely that these animals were photorefractory. The absence
of an inhibitory effect of LDs on the reproductive status of males and
females of all species suggests that the seasonal reproductive patterns of these rodents may not be photoperiodically regulated in the wild.
Nevertheless, the inhibitory effect of SDs on male reproductive status
indicates that these animals can discriminate SDs from LDs. When the
possible relations between tropical mammals and photoperiodism (20) are
extended to these and perhaps other desert rodents, it would appear
that they are moderately photoresponsive but that they may not use day
length as the primary proximal cue to trigger reproductive and other
seasonal responses. Although the annual variation in day lengths in
Egypt is sufficient to permit dependence on the photoperiod as a
proximate factor to regulate reproduction and other seasonal changes
(5), it might not be expected that desert rodents depend on the
photoperiod to cue their reproduction given the harsh, unpredictable
climate of the desert (7). Therefore, a possible explanation for the present results is that photoperiodic inhibition of reproduction may be
overridden by other factors in their natural habitat that allow
breeding to coincide with the rainy season when food is abundant. This
suggestion parallels findings on California voles (Microtus
californicus), another
winter-breeding species (33). In the laboratory, male California voles
undergo gonadal regression in SDs, but the ingestion of green
vegetation overrides the inhibitory influence of SD exposure.
Furthermore, it is possible that the inhibitory effect of SDs reported
in the present investigation may be overridden in the natural habitat
by social cues. The role of social cues in regulating reproduction has
been observed in many rodent species (for review, see Ref. 7). For
example, the presence of females enhances male reproductive functions
under LD conditions in some species (12) and overrides the inhibitory reproductive effects of SD exposure in other species (45, 46).
In the present study there was individual variation in the rates of
testicular regression within the same species and between different
species. Such variation in reproductive responsiveness to SDs has been
seen in many other species and is thought to be genetically based (13,
21, 32) but may be environmentally triggered (17).
Testes of animals with access to running wheels had significantly
increased spermatogenic activity compared with their sedentary counterparts. These results are consistent with stimulation of reproductive functions of other photoperiodic and nonphotoperiodic rodent species by exercise (8, 26, 27, 37, 46). The underlying
mechanism for this effect is not precisely known, but the
hypothalamic-pituitary-gonadal axis may be involved (26, 27). Although
the changes in spermatogenic activity reported in the present study
between wheel running and sedentary animals were not robust, it may be
significant to the animals in the wild and could indicate the
possibility that locomotor activity antagonizes the inhibitory effect
of SDs on reproductive functions.
In many rodent species, the photoperiod affects female and male
reproductive status similarly. For example, exposure of male Siberian
hamsters to SDs decreases testes and uterine masses as well as
eliminates ovarian corpora lutea and antral follicles (43, 44). This
was not found in the present study, where the ovaries of LD- and
SD-housed animals of all species exhibited well-developed antral
follicles and corpora lutea, although their male counterparts underwent
partial gonadal regression. It is not known why females in these
species differ from males in lacking even mild reproductive photoresponsiveness.
In summary, the present study demonstrates that some desert rodent
species are responsive to the photoperiod but that changes in the
photoperiod alone are not enough to induce robust changes in
reproductive responses. Therefore, it is suggested that alterations in
the day length cannot, in and of themselves, account for the seasonal
reproductive cycles seen by these species in the wild.
Perspectives
The environmental factors that regulate the reproductive patterns of
desert rodents in the wild remain to be identified. There is some
evidence that desert rodents generally curtail breeding during the dry
season and breed only during the rainy season in the following months
when desert grasses are abundant (19). One possible outcome of this
scenario is that desert rodents use the ingestion of green food for
timing their reproduction (for review, see Ref. 7). Reliance on a
secondary plant compound (e.g., 6-methoxy-2-benzoxazolinone) found in
young grasses and sedges to predict oncoming periods of maximum food
availability, and thus conditions favorable for reproduction, has been
documented in other species of small mammals (1, 42). Desert rodents could use such plant predictors in timing their reproduction with or
without photoperiodic regulation (7). Strict reliance on the
photoperiod as a predictor for timing the reproductive season, however,
could be disadvantageous in desert environments in which climatic and
nutritional conditions change in an unpredictable manner (10). Because
of the harsh desert environment, reproduction in desert species may not
be successful in any given year (25), suggesting that desert rodents
breed opportunistically depending on relatively short-term climatic and
nutritional conditions without using any predictors. In addition, they
also may have overcome some of their reproductive difficulties by being
long-lived. Although there are no available field data, this may be the
case for our animals. For example, longevity of a captive specimen of
Gerbillus pyramidum was 8.17 yr
(reviewed in Ref. 34). Taken together, the results of the present study
suggest that photoperiod may play a role in seasonal breeding in some
desert rodents, although other environmental factors also may
contribute to the seasonal breeding seen in the wild.
| |
ACKNOWLEDGEMENTS |
We thank Drs. Bruce Goldman and Gregory Demas for insightful
discussions of the data and comments on the manuscript. We are grateful
to Dr. Eric Mintz for helping with the statistics. We also thank the
Egyptian Government Scholarship Program for their support.
| |
FOOTNOTES |
This work was supported, in part, by National Institute of Mental
Health Grants R01-MH-48473 and RSDA-K02-MH-00841 and National Institute
of Diabetes and Digestive and Kidney Diseases Grant R01-DK-35254 to T. J. Bartness.
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests: T. J. Bartness, Depts. of Psychology and
Biology, Georgia State Univ., Univ. Plaza, Atlanta, GA 30303.
Received 22 June 1998; accepted in final form 26 August 1998.
| |
REFERENCES |
1.
Alibhai, S. K.
Reproductive response of Gerbillus harwoodii to 6-MBOA in the Kora National Reserve, Kenya.
J. Trop. Pediatr.
2:
377-379,
1986.
2.
Bartness, T. J.
Animal and body fat changes: measurement and interpretation.
In: Methods and Techniques to Study Feeding and Drinking Behavior, edited by F. M. Toates,
and N. E. Rowland. Amsterdam: Elsevier, 1987, p. 463-498.
3.
Bartness, T. J.,
and
B. D. Goldman.
Mammalian pineal melatonin: a clock for all seasons.
Experientia
45:
939-945,
1989[Medline].
4.
Bartness, T. J.,
and
G. N. Wade.
Seasonal body weight cycles in hamsters.
Neurosci. Biobehav. Rev.
9:
599-612,
1985[Medline].
5.
Beck, S. D.
Insect Photoperiodism. New York: Academic, 1968.
6.
Borer, K. T.,
C. S. Campbell,
J. Tabor,
K. Jorgenson,
S. Kandarian,
and
L. Gordon.
Exercise reverses photoperiodic anestrus in golden hamsters.
Biol. Reprod.
29:
38-47,
1983[Abstract].
7.
Bronson, F. H.
Mammalian reproduction: an ecological perspective.
Biol. Reprod.
32:
1-26,
1985[Abstract].
8.
Bronson, F. H.
Puberty in female rats: relative effect of exercise and food restriction.
Am. J. Physiol.
252 (Regulatory Integrative Comp. Physiol. 21):
R140-R144,
1987[Abstract/Free Full Text].
9.
Bronson, F. H.
Mammalian Reproductive Biology. Chicago: University of Chicago Press, 1989.
10.
Bronson, F. H.,
and
P. D. Heideman.
Seasonal regulation of reproduction in mammals.
In: The Physiology of Reproduction, edited by E. Knobil,
and J. D. Neill. New York: Raven, 1994, p. 541-583.
11.
Conley, W.,
J. D. Nichols,
and
A. R. Tipton.
Reproductive strategies in desert rodents.
In: Transactions of the Symposium on the Biological Resources of the Chihuahuan Desert Region, edited by R. H. Wauer,
and D. H. Riskind. Washington, DC: US Printing Office, 1974, p. 193-214.
12.
Demas, G. E.,
and
R. J. Nelson.
Social, but not photoperiodic, influences on reproductive function in male Peromyscus aztecus.
Biol. Reprod.
58:
385-389,
1998[Abstract/Free Full Text].
13.
Desjardins, C.,
F. H. Bronson,
and
J. L. Blank.
Genetic selection for reproductive photoresponsiveness in deer mice.
Nature
322:
172-173,
1986[Medline].
14.
Duncan, M. J.,
and
B. D. Goldman.
Hormonal regulation of the annual pelage cycle in the Djungarian hamster, Phodopus sungorus. II. Role of prolactin.
J. Exp. Zool.
230:
97-103,
1984[Medline].
15.
Evered, D.,
and
S. Clark.
Photoperiodism, Melatonin and the Pineal: Ciba Foundation Symposium 117. London: Pitman, 1985, p. 1-323.
16.
Gibbs, F. P.,
and
L. J. Petterborg.
Exercise reduces gonadal atrophy caused by short photoperiod or blinding of hamsters.
Physiol. Behav.
37:
159-162,
1986[Medline].
17.
Gorman, M. R.,
and
I. Zucker.
Environmental induction of photononresponsiveness in the Siberian hamster, Phodopus sungorus.
Am. J. Physiol.
272 (Regulatory Integrative Comp. Physiol. 41):
R887-R895,
1997[Abstract/Free Full Text].
18.
Grocock, C. A.,
and
J. R. Clarke.
Photoperiodic control of testis activity in the vole, Microtus agrestis.
J. Reprod. Fertil.
39:
337-347,
1974[Medline].
19.
Happold, D. C. D.
The ecology of rodents in the northern Sudan.
In: Rodents in Desert Environments, edited by I. Prakash,
and P. K. Ghosh. The Hague: Dr. W. Junk, 1975, p. 15-25.
20.
Heideman, P. D.,
and
F. H. Bronson.
Photoperiod, melatonin secretion and sexual maturation in a tropical rodent.
Biol. Reprod.
43:
745-750,
1990[Abstract].
21.
Heideman, P. D.,
and
F. H. Bronson.
Characteristics of a genetic polymorphism for reproductive photoresponsiveness in the white-footed mouse (Peromyscus leucopus).
Biol. Reprod.
44:
1189-1196,
1991[Abstract].
22.
Heldmaier, G.,
S. Steinlechner,
J. Rafael,
and
P. Vsiansky.
Photoperiodic control and effects of melatonin on nonshivering thermogenesis and brown adipose tissue.
Science
212:
917-919,
1981[Abstract/Free Full Text].
23.
Hoogstraal, H. A.,
K. Wassif,
and
M. N. Kaiser.
Results of the Namru-3 Southeastern Egypt Expedition, 1954. 6. Observations of non-domesticated mammals and their ectoparasites.
Bull. Zool. Soc. Egypt
13:
52-75,
1957.
24.
Kenagy, G. J.,
and
G. A. Bartholomew.
Effects of daylength, temperature and green food on testicular development in a desert pocket mouse Perognathus formosus.
Physiol. Zool.
54:
62-73,
1981.
25.
Kenagy, G. J.,
and
G. A. Bartholomew.
Seasonal reproductive patterns in five coexisting California desert rodent species.
Ecol. Monogr.
55:
371-397,
1985.
26.
Kerbeshian, M. C.,
and
F. H. Bronson.
Running-induced testicular recrudescence in the meadow vole: role of the circadian system.
Physiol. Behav.
60:
165-170,
1996[Medline].
27.
Kerbeshian, M. C.,
H. LePhuoc,
and
F. H. Bronson.
The effects of running activity on the reproductive axes of rodents.
J. Comp. Physiol. [A]
174:
741-746,
1994[Medline].
28.
Khammar, F.,
and
R. Brudieux.
Seasonal changes in testicular contents of testosterone and androstenedione and in the metabolic clearance rate of testosterone in the sand rat (Psammomys obesus).
J. Reprod. Fertil.
71:
235-241,
1984[Abstract].
29.
Khammar, F.,
and
R. Brudieux.
Seasonal changes in testicular contents and plasma concentrations of androgens in the desert gerbil.
J. Reprod. Fertil.
80:
589-594,
1987[Abstract].
30.
Leshner, A. I.,
V. A. Litwin,
and
R. L. Squibb.
A simple method for carcass analysis.
Physiol. Behav.
9:
281-282,
1972[Medline].
31.
Lincoln, G. A.,
and
R. V. Short.
Seasonal breeding: nature's contraceptive.
Recent Prog. Horm. Res.
3:
1-52,
1980.
32.
Lynch, G. R.,
C. B. Lynch,
and
R. Kliman.
Genetic analyses of photononresponsiveness in the Djungarian hamster, Phodopus sungorus.
J. Comp. Physiol. [A]
164:
475-481,
1989[Medline].
33.
Nelson, R. J.,
J. Dark,
and
I. Zucker.
Influence of photoperiod, nutrition and water availability on male California voles (Microtus californicus).
J. Reprod. Fertil.
69:
473-477,
1983[Abstract].
34.
Nowak, R. M.
Walker's Mammals of the World. Baltimore, MD: Johns Hopkins University Press, 1991, p. 727-739.
35.
Osborn, D. J.,
and
I. Helmy.
The Contemporary Land Mammals of Egypt (Including Sinia). Chicago: Field Museum Natural History, 1980, p. 94-323.
36.
Pedersen, T.,
and
H. Peters.
Proposal for a classification of oocytes and follicles in the mouse ovary.
J. Reprod. Fertil.
17:
555-557,
1968[Medline].
37.
Perrigo, G.,
and
F. H. Bronson.
Foraging effort, food intake, fat deposition, and puberty in female mice.
Biol. Reprod.
29:
455-463,
1983[Abstract].
38.
Pieper, D. R.,
H. Y. Ali,
L. L. Benson,
M. D. Shows,
C. A. Lobocki,
and
M. G. Subramanian.
Voluntary exercise increases gonadotropin secretion in male Golden hamsters.
Am. J. Physiol.
269 (Regulatory Integrative Comp. Physiol. 38):
R179-R185,
1995[Abstract/Free Full Text].
39.
Pieper, D. R.,
K. T. Borer,
C. A. Lobocki,
and
D. Samuel.
Exercise inhibits reproductive quiescence induced by exogenous melatonin in hamsters.
Am. J. Physiol.
255 (Regulatory Integrative Comp. Physiol. 24):
R718-R723,
1988[Abstract/Free Full Text].
40.
Prakash, I.,
and
P. K. Ghosh.
Rodents in Desert Environment. The Hague: Dr. W. Junk, 1975.
41.
Reichman, O. J.,
and
K. M. Van de Graff.
Seasonal activity and reproductive patterns of five species of Sonoran desert rodents.
Am. Midl. Nat.
90:
118-126,
1973.
42.
Sanders, E. H.,
P. D. Gardner,
P. J. Berger,
and
N. C. Negus.
6-Methoxybenzoxazolinone: a plant derivative that stimulates reproduction in Microtus montanus.
Science
214:
67-67,
1981[Free Full Text].
43.
Schlatt, S.,
P. Niklowitz,
K. Hoffmann,
and
E. Nieschlag.
Influence of short photoperiods on reproductive organs and estrous cycles of normal and pinealectomized female Djungarian hamsters, Phodopus sungorus.
Biol. Reprod.
49:
243-250,
1993[Abstract].
44.
Wade, G. N.,
and
T. J. Bartness.
Effects of photoperiod and gonadectomy on food intake, body weight, and body composition in Siberian hamsters.
Am. J. Physiol.
246 (Regulatory Integrative Comp. Physiol. 15):
R26-R30,
1984[Abstract/Free Full Text].
45.
Wayne, N. L.,
and
E. F. Rissman.
Effects of photoperiod and social variables on reproduction and growth in the male shrew (Suncus murinus).
J. Reprod. Fertil.
89:
707-715,
1990[Abstract].
46.
Whitsett, J. M.,
and
A. D. Lawton.
Social stimulation of reproductive development in male deer mice housed on a short-day photoperiod.
J. Comp. Physiol. [A]
96:
416-422,
1982.
47.
Zaime, A.,
M. Laraki,
J. Gautier,
and
D. H. Garnier.
Seasonal variations of androgens and of several sexual parameters in male Meriones shawi in southern Morocco.
Gen. Comp. Endocrinol.
86:
289-296,
1990.
Am J Physiol Regul Integr Compar Physiol 275(6):R2012-R2022
0002-9513/98 $5.00
Copyright © 1998 the American Physiological Society
Top
Abstract
Introduction
