Climate change and seasonal reproduction in mammals.

Seasonal reproduction is common among mammals at all latitudes, even in the deep tropics. This paper (i) discusses the neuroendocrine pathways via which foraging conditions and predictive cues such as photoperiod enforce seasonality, (ii) considers the kinds of seasonal challenges mammals actually face in natural habitats, and (iii) uses the information thus generated to suggest how seasonal reproduction might be influenced by global climate change. Food availability and ambient temperature determine energy balance, and variation in energy balance is the ultimate cause of seasonal breeding in all mammals and the proximate cause in many. Photoperiodic cueing is common among long-lived mammals from the highest latitudes down to the mid-tropics. It is much less common in shorter lived mammals at all latitudes. An unknown predictive cue triggers reproduction in some desert and dry grassland species when it rains. The available information suggests that as our climate changes the small rodents of the world may adapt rather easily but the longer lived mammals whose reproduction is regulated by photoperiod may not do so well. A major gap in our knowledge concerns the tropics; that is where most species live and where we have the least understanding of how reproduction is regulated by environmental factors.

Are humans seasonally photoperiodic?

Humans exhibit seasonal variation in a wide variety of behavioral and physiological processes, and numerous investigators have suggested that this might be because we are sensitive to seasonal variation in day length. The evidence supporting this hypothesis is inconsistent. A new hypothesis is offered here-namely, that some humans indeed are seasonally photoresponsive, but others are not, and that individual variation may be the cause of the inconsistencies that have plagued the study of responsiveness to photoperiod in the past. This hypothesis is examined in relation to seasonal changes in the reproductive activity of humans, and it is developed by reviewing and combining five bodies of knowledge: correlations of human birthrates with photoperiod; seasonal changes in the activity of the neuroendocrine pathway that could link photoperiod to gonadal steroid secretion in humans; what is known about photoperiod, latitude, and reproduction of nonhuman primates; documentation of individual variation in photoresponsiveness in rodents and humans; and what is known about the evolutionary ecology of humans.

Puberty in female mice is not associated with increases in either body fat or leptin.

It has been hypothesized that puberty is triggered when body fat and hence circulating levels of leptin exceed critical thresholds. Four kinds of experiments tested that hypothesis in female mice. When age was the independent variable, body fat and circulating levels of leptin decreased rather than increased before the onset of puberty. When stage of reproductive development was the independent variable, neither body fat nor circulating levels of leptin correlated with the onset of puberty. In sharp contrast, reproductive development was well correlated with body weight. A significant nocturnal peak in circulating levels of leptin was seen before and at all stages of reproductive development, but the highest levels were seen after rather than before the first estrous cycle was initiated. Neither acceleration nor deceleration of puberty by varying the female's social environment had any effect on either body fat or leptin. There is no support in any of these experiments for the hypothesis that an increase in body fat and thus an increase in circulating levels of leptin triggers puberty in female mice.

Energy balance and ovulation: small cages versus natural habitats.

In the laboratory, ovulation is suppressed when a mammal is in negative energy balance whether that state is caused by inadequate food intake, excessive locomotor activity or heavy thermoregulatory costs. In this paper, knowledge generated in the laboratory about the link between ovulation and energy balance is examined in relation to the kinds of energetic challenges mammals actually face in natural habitats. When viewed in that context, several conclusions can be drawn. First, females ovulate whenever extant energetic conditions permit unless the process is blocked by non-metabolic stress, social cues or a predictive seasonal cue such as photoperiod. In the latter case, most mammals show at least a seasonal tendency in their reproduction and the majority do not use a predictive cue; they reproduce opportunistically in relation to seasonal variation in the energetic characteristics of their environment. Second, the widely held assumption that a female's fat reserves must exceed a critical level in order that she may ovulate finds no support in the literature dealing with natural populations. Third, the surprisingly rapid responsiveness of the gonadotrophin releasing hormone (GnRH) pulse generator to energetic manipulation probably reflects the study of animals that are in a pure survival mode. Fourth, the complexity of the energetic challenges mammals face in the wild suggests that there are probably multiple metabolic and neural pathways coupling ovulation to energy balance and that these pathways are probably characterized by considerable overlap and redundancy. Thus, fifth, to develop a more realistic overview of these pathways there is a need for experimental designs that present mammals with the kinds of complex challenges they actually face in the wild habitats in which they evolved.

Exposure to anabolic-androgenic steroids shortens life span of male mice.

Adult male laboratory mice were exposed for 6 months to a combination of four anabolic-androgenic steroids of the kinds and at the relative levels to which human athletes and body builders expose themselves. The four steroids included testosterone, two 17-alkylated steroids, and an ester, and they were given at doses that totaled either 5 or 20 times normal androgenic maintenance levels for mice. By the time the survivors were 20 months old (1 yr after the termination of steroid exposure), 52% of the mice given the high dose of steroids had died compared with 35% of the mice given the low dose and only 12% of the control mice given no exogenous hormones (P < 0.001). Autopsy of the steroid-treated mice typically revealed tumors in the liver or kidney, other kinds of damage to these two organs, broadly invase lymphosarcomas, or heart damage, and usually more than one of these conditions. It can be concluded that the life span of male mice is decreased dramatically by exposing them for 6 months to the kinds and relative levels of anabolic steroids used by many athletes and body builders.

Running-induced testicular recrudescence in the meadow vole: role of the circadian system.

Access to running wheels stimulates testicular recrudescence in meadow voles whose reproductive axes have been suppressed by short day lengths. The present experiments addressed the mechanism by which running stimulates the reproductive system. The results from two experiments suggest that running acts specifically to override the short day length suppression of the gonads: access to running wheels had no stimulatory effect on the testes of meadow voles housed in long day lengths, and the degree to which running stimulated the testes of meadow voles housed under short day lengths was significantly correlated with the degree to which the voles were reproductively photoresponsive. A third experiment queried whether running shifts the circadian clock in such a way as to cause an overlap between the short day length photoperiod and the period of sensitivity to light. This proved not to be the case: access to running wheels stimulated testicular recrudescence in meadow voles housed in constant darkness. Two experiments demonstrated that access to a running wheel did not alter short day length profiles of pineal melatonin content or the nocturnal rise in pineal melatonin content in the absence of light. Finally, daily patterns of circulating corticosterone levels did differ between voles with and without access to running wheels, although the difference could not be attributed to differences in the circadian system. Overall, these experiments suggest that running stimulates gonadal recrudescence by acting on the pathway by which photoperiod suppresses reproduction downstream of melatonin production.

Melatonin rhythms and pineal structure in a tropical bat, Anoura geoffroyi, that does not use photoperiod to regulate seasonal reproduction.

It has been hypothesized that pineal structure and function might differ between temperate zone and tropical species of mammals because of lower amplitudes of seasonal change in photoperiod and, in some areas, less seasonal climatic variation. Anoura geoffroyi produce a single offspring in November or December of each year on the Caribbean island of Trinidad, at 10 degrees N latitude in the deep tropics. Previous work has shown that this population lacks reproductive responses to photoperiod, and must be enforcing seasonal breeding using a non-photoperiodic cue. Anoura geoffroyi have a minute, thin, and rod-like pineal gland. Throughout much of its length, the pineal courses irregularly within the ventrolateral wall of the great cerebral vein. This intimate relationship may have functional implications. Despite having a very small pineal gland, this species produced a nocturnal rise in serum melatonin. Serum melatonin levels in most individuals were below or near undetectable levels during the light period and rose to a peak averaging 100 pg/ml in the last third of the dark period. Our results indicate that, although the pineal gland of A. geoffroyi is extremely small, serum melatonin levels are comparable to those of other mammals.

Melatonin rhythms and pineal structure in a tropical bat, Anoura geoffroyi, that does not use photoperiod to regulate seasonal reproduction

It has been hypothesized that pineal structure and function might differ between temperature zone and tropical species of mammals because of lower amplitudes of seasonal change in photoperiod and, in some areas, less seasonal climatic variation. Anoura geoffroyi produce a single offspring in November or December of each year on the Caribbean island of Trinidad, at 10 degrees N latitude in the deep tropics. Previous work has shown that this population lacks reproductive responses to photoperiod, and must be enforcing seasonal breeding using a non-photoperiodic cue. Anoura geoffroyi have a minute, thin, and rod-like pineal gland. Throughout much of its length, the pineal courses irregularly within the ventrolateral wall of the great cerebral vein. This intimate relationship may have functional implications. Despite having a very small pineal gland, this species produced a nocturnal rise in serum melatonin. Serum melatonin levels in most individuals were below or near undetectable levels during the light period and rose to a peak averaging 100 pg/ml in the last third of the dark period. Our results indicate that, although the pineal gland of A. geoffroyi is extremely small, serum melatonin levels are comparable to those of other mammals.(AU)

Effects of prolonged exposure to anabolic steroids on the behavior of male and female mice.

Adult male and female mice were exposed to a combination of four anabolic-androgenic steroids at pharmacological doses for 6 months. Males were exposed to either 5 or 20 times androgenic maintenance levels, as determined by bioassay; females were exposed to either one or five times the maintenance levels for males. Even the low doses were sufficient to reduce gonadal weight in both sexes and eliminate the estrous cycle in females. Steroid treatment blocked ejaculation in most males without influencing other facets of their sexual behavior. In some females steroid treatment elicited male-like mounting and pelvic thrusting. Exposure to steroids increased aggressiveness in females. Using a different testing protocol, steroid exposure had no effect on aggressiveness in males. Steroid treatment decreased the use of a running wheel significantly in females and marginally in males. Overall, the results of this experiment suggest no enhancement of normal androgen-mediated behavior in males, but potent effects on the behavior of females.

Effect of anabolic steroids on behavior and physiological characteristics of female mice.

Adult female mice were exposed to a combination of four anabolic-androgenic steroids for 9 weeks at doses that were either one or five times the androgenic maintenance level for male mice. Relative to control females, steroid treatment depressed gonadotropin secretion and increased both dry body weight and fat content but without an increase in food intake. Steroid treatment depressed spontaneous use of a running wheel and open-field activity, and it increased aggressiveness. It also eliminated a behavior related to encounters between the sexes--the rejection of genital inspection. There was no effect of steroid treatment on the time required to recover from 10 h of enforced running on a treadmill. Overall, regardless of the test or measure, there was little or no difference in the effect of the high and low dose of steroids. This indicates a threshold of response below the low dose used in these studies, which itself is probably well below that used by many female athletes and body builders.

Seasonal variation in human reproduction: environmental factors.

Almost all human populations exhibit seasonal variation in births, owing mostly to seasonal variation in the frequency of conception. This review focuses on the degree to which environmental factors like nutrition, temperature and photoperiod contribute to these seasonal patterns by acting directly on the reproductive axis. The reproductive strategy of humans is basically that of the apes: Humans have the capacity to reproduce continuously, albeit slowly, unless inhibited by environmental influences. Two, and perhaps three, environmental factors probably act routinely as seasonal inhibitors in some human populations. First, it seems likely that ovulation is regulated seasonally in populations experiencing seasonal variation in food availability. More specifically, it seems likely that inadequate food intake or the increased energy expenditure required to obtain food, or both, can delay menarche, suppress the frequency of ovulation in the nonlactating adult, and prolong lactational amenorrhea in these populations on a seasonal basis. This action is most easily seen in tropical subsistence societies where food availability often varies greatly owing to seasonal variation in rainfall; hence births in these populations often correlate with rainfall. Second, it seems likely that seasonally high temperatures suppress spermatogenesis enough to influence the incidence of fertilization in hotter latitudes, but possibly only in males wearing clothing that diminishes scrotal cooling. Since most of our knowledge about this phenomenon comes from temperate latitudes, the sensitivity of spermatogenesis in both human and nonhuman primates to heat in the tropics needs further study. It is quite possible that high temperatures suppress ovulation and early embryo survival seasonally in some of these same populations. Since we know less than desired about the effect of heat stress on ovulation and early pregnancy in nonhuman mammals, and nothing at all about it in humans or any of the other primates, this is an important area for future research. Third, correlational data suggest that there may be some degree of regulation of reproduction by photoperiod in humans at middle to higher latitudes. Populations at these latitudes often show a peak in presumed conceptions associated with the vernal equinox. On the other hand, evidence gathered by neuroendocrinologists tends to argue against reproductive photoresponsiveness in humans.

Tonic-clonic convulsions in meadow voles.

Some meadow voles (Microtus pennsylvanicus) exhibit prolonged tonic-clonic convulsions, possibly epileptiform seizures, when handled or exposed to a strange environment. These convulsions are often preceded by a period of slow head shaking and/or stiff-legged hopping, but never by the explosively wild running bouts that characterize convulsions in some mammals. Convulsions occasionally occur in meadow voles in response to mild disturbance, as when an individual in its home cage is carried from one room to another. In contrast, they can not be elicited by some of the auditory or olfactory insults used to induce epileptiform seizures in other mammals. Breeding experiments have established the genetic basis of the convulsions seen in meadow voles, and of particular interest here is the fact that some of the convulsing voles were caught in the wild. This raises the interesting possibility that wild voles in natural habitats might be susceptible to convulsions when startled.

The effects of running activity on the reproductive axes of rodents.

Access to a running wheel causes gonadal recrudescence in Syrian hamsters whose reproductive axes have been suppressed by housing them under short day lengths (Borer et al. 1983). The first experiment tested the generality of this phenomenon in a population of rodents that is genetically heterogeneous for reproductive photoresponsiveness. Male meadow voles (Microtus pennsylvanicus) of the two extreme phenotypes--reproductively photoresponsive and non-responsive--were either provided with a running wheel or housed without one. After 4 weeks with a wheel, the responsive voles had recovered full reproductive function, while the reproductive axes of responsive voles housed without wheels remained suppressed. Three experiments queried whether the use of a wheel would have reproductively stimulative effects in other rodents. First, intact male mice given access to wheels showed no increase in testis size when compared to mice housed without wheels. Likewise, locomotor activity had no effect on male rats whose testes were partially regressed in response to testosterone implants or on female mice whose estrous cycles were pheromonally suppressed by housing them in groups. Thus the neuroendocrine pathway used by locomotor activity to enhance the secretion of gonadotropin is specifically allied with the pathway used by photoperiod to control GnRH secretion.

Variation in reproductive photoresponsiveness in a wild population of meadow voles.

Individual variation in reproductive photoresponsiveness has been documented in laboratory colonies of several species of rodents. When maintained on short day lengths, some individuals experience complete gonadal regression, others undergo little if any gonadal regression, and still others show intermediate levels of responsiveness. In the present research, a combination of laboratory and field studies explored the potential importance of this kind of variation for the control of seasonal breeding in a wild population of meadow voles (Microtus pennsylvanicus). A sample of adult males was trapped in central Pennsylvania during the summer when all were in breeding condition. When exposed to short day lengths in the laboratory, these males showed the entire range of variation in responsiveness noted above and, correlatively, variation in the loss in body weight induced by this treatment. A sample of males trapped in the wild just before the winter solstice showed the same distribution of variation as did the males housed on short day lengths in the laboratory, and thus, as might be expected, a few pregnant and lactating females were also trapped at this time. Longitudinal studies over a 42-wk period revealed that the variation reflects the degree to which the testes regress in response to short-day exposure rather than the rate at which they regress. Finally, studies with laboratory-born voles demonstrated that the variation is independent of age. In total, these studies demonstrate that the variation in reproductive photoresponsiveness previously seen only in laboratory colonies of rodents indeed has relevance for understanding the seasonal control of reproduction in the wild.

An endogenous circannual rhythm of reproduction in a tropical bat, Anoura geoffroyi, is not entrained by photoperiod.

Most species of mammals live in the tropics, and many breed seasonally, but little is known about the regulation of their seasonal cycles. Males of a tropical bat, Anoura geoffroyi (Order Chiroptera, Family Phyllostomidae), from 10 degrees latitude in Trinidad, were studied to test the role of photoperiod in regulating seasonal reproduction in the deep tropics. Groups of males were subjected to five treatments: 1) constant photoperiod; 2) a 12-mo cycle of civil twilight photoperiods mimicking those occurring at 10 degrees latitude; 3) civil twilight photoperiods of 10 degrees latitude, but accelerated to a 9-mo cycle; 4) civil twilight photoperiods characteristic of 30 degrees latitude, but accelerated to a 9-mo cycle; and 5) constant photoperiod, but with the timing of dark onset varied to match the timing of darkness at 10 degrees latitude, and accelerated to a 9-mo cycle. In all treatments, the first cycle of testis growth and regression matched that expected in the wild population, as reported previously for some of these groups. Subsequently, the testis cycle of bats in constant conditions free-ran for 20 mo with a peak-to-peak period of 7.3 +/- 0.3 mo. Period lengths in the four nonconstant groups, 7.2-7.7 mo, were not significantly different from that under constant conditions. Bats failed to entrain to any photoperiod cycle, including those mimicking changes at 10 degrees or 30 degrees latitude. They also failed to entrain to the cycle in which day length was held constant while time of sunset was varied, as occurs at the equator.(ABSTRACT TRUNCATED AT 250 WORDS)

Correlation between reproductive photoresponsiveness and photoregulated locomotor activity in meadow voles.

Some rodent populations contain individuals that undergo complete gonadal regression under short day lengths, other individuals whose gonads are little affected by such treatment, and still others that are intermediate in their response. Meadow voles exhibiting this variation were used to explore the relationship between reproductive photoresponsiveness and photoregulated locomotor activity. The activity patterns of the two extreme phenotypes--reproductively photoresponsive vs. nonresponsive--were compared, first under short day lengths and then under long day lengths. The primary component of the daily running wheel activity pattern for both phenotypes under both conditions was ultradian. Within that framework, reproductively photoresponsive voles were predominantly nocturnal in their locomotor activity under both day lengths. In contrast, the nonresponsive individuals showed no significant circadian variation in their activity under either day length. These results suggest that reproductively photoresponsive and nonresponsive individuals may have fundamentally different patterns of activity throughout the year in the wild. Furthermore, the data suggest that the inability of some voles to respond reproductively to variations in photoperiod may be caused by a decoupling of the circadian system from the entraining effects of day length.

Failure of cryptorchidism to suppress fertility in a tropical rodent.

The cane mouse (Zygodontomys brevicauda) breeds year-round on the hot llanos of Venezuela, only 8 degrees above the equator. The reproductive responses of the males of this species to heat were compared with those of a temperature zone rodent, the white-footed mouse (Peromyscus leucopus). When tested at different ambient temperatures, the movement of the testis in relation to the scrotum was similar in the two species, but the cane mouse's testis proved to be much more resistant to maintenance at core body temperature. In two experiments, cryptorchid cane mice experienced only a 24% and a 5% decrease in testis weight, and almost all of these males showed normal spermatogenesis and sperm storage. In comparison, cryptorchid white-footed mice showed a 58% drop in testis weight, a total inhibition of spermatogenesis, and a complete or near absence of stored sperm in all males. A mating test demonstrated that cane mice indeed remain fertile for at least 2 to 3 mo after being rendered cryptorchid. Normal numbers of these males when paired with females fathered normal litters. It is noted that the relative insensitivity of the testis of the cane mouse to heat might actually be more representative of scrotal mammals in general than is suggested by our present perspective, which has been developed on the basis of study of humans and mammals from cool climates rather than the tropics, where most mammals live.

Sensitivity of Syrian hamsters (Mesocricetus auratus) to amplitudes and rates of photoperiodic change typical of the tropics.

Empirical data suggest that reproductive photoresponsiveness occurs in some populations of mammals above 13 degrees of latitude, but may be absent in populations from 0 degrees to 10 degrees of latitude. The present experiments examined the degree to which the low amplitude of change in photoperiod in the tropics constrains mammals from using daylength as a seasonal cue. The Syrian hamster, a temperate-zone species, was studied because of its well-documented ability to respond to small changes in photoperiod, and because of the absence of an alternative robustly responding species from the tropics. We subjected adult male hamsters to photoperiods that mimicked the amplitude and rate of photoperiod change of 30 degrees, 20 degrees, 10 degrees, and 5 degrees of latitude, but centered around an estimate of their critical daylength. For comparison, a fifth group was subjected to an abrupt change in daylength of a magnitude equal to the total annual variation occurring at 30 degrees. The two groups experiencing the gradually changing daylengths of 30 degrees and 20 degrees showed less within-group synchrony during testicular regression; in other dimensions of the annual testis cycle, including the degree of synchrony exhibited during recrudescence, they reacted similarly to the hamsters given the abrupt change in daylength. Some of the hamsters exposed to the gradually changing daylengths of 10 degrees responded to this challenge, as did a few in the 5 degrees treatment--in both cases, with poor within-group synchrony and a submaximal decrease in testis size. In an abbreviated second experiment, hamsters given abrupt decreases in daylength of magnitudes equal to those of the 10 degrees and 5 degrees groups responded slightly more frequently, and with maximal decreases in testis size. This suggests that mammals may not be constrained absolutely by an inability to respond to changes in photoperiod at 5 degrees to 10 degrees latitude. Seasonally breeding populations of mammals in the deep tropics that do not use photoperiod to regulate reproduction may use nonphotoperiodic cues because they offer a higher signal-to-noise ratio than do tropical changes in photoperiod.

Seasonal reproduction of a tropical bat, Anoura geoffroyi, in relation to photoperiod.

Anoura geoffroyi (Chiroptera, Phyllostomidae, Glossophaginae), Geoffroy's hairy-legged long-tongued bat, were collected from September 1984 to August 1985, and these bats were found to breed seasonally in the wild on Trinidad, West Indies, at 10 degrees N latitude. Histological examination of these samples indicated that females became pregnant in July or August, and young were born in late November or early December. The testes and epididymides were small from September to mid-April, increased threefold in weight between mid-April and late May, reached a peak weight in July, and decreased in weight in August. Spermatogenesis occurred throughout the testes of males captured from May to August. In 1990, the timing of parturition in females that gave birth in the laboratory to young conceived in the wild was similar to the timing in the field in 1984-1985. Groups of 10-13 males were subjected in the laboratory to (i) a gradually changing, civil twilight photoperiod that mimicked the natural cycle of annual change at 10 degrees N latitude, (ii) the same gradually changing cycle of photoperiod accelerated to a six-month period, or (iii) a constant photoperiod (light 12:54 h: dark 11:06 h). These treatments began in mid-December, four months before the initiation of testicular recrudescence in the wild. In all three groups, testicular volume remained low until April, and then increased two- to threefold between late April and late June, rising to a peak in July, as occurred in the wild.(ABSTRACT TRUNCATED AT 250 WORDS)

Life history and bioeconomy of the house mouse.

1. More is known about the western European house mouse, Mus (musculus) domesticus than any other non-human mammal. If laboratory and field information is combined, an extremely valuable understanding of the species' bioeconomy could be obtained. 2. The seven stages of mouse life-history are surveyed (up to birth, nest life, sex life, social structure, population statics and stability, senescence, and death), and the interactions between the changing phenotype and the environment are described. 3. These interactions can be used to build up a model of the opportunities and compromises which result in the fitness of individual mice. It is not yet possible to quantify such a model, but this should in principle be achievable.