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Biology of Reproduction 60, 1320-1323 (1999)
©Copyright 1999 Society for the Study of Reproduction, Inc.

Articles

Short Day Length Alone Does Not Inhibit Spermatogenesis in the Seasonally Breeding Four-Striped Field Mouse (Rhabdomys pumilio)1

C. Jacksona, and R.T.F. Bernard2,a

a Department of Zoology & Entomology, Rhodes University, Grahamstown 6139, South Africa


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
This study was an examination of the effect of photoperiod on spermatogenesis and the accessory glands of the four-striped field mouse (Rhabdomys pumilio), a seasonally breeding rodent that occurs through Southern Africa. Adult scrotal males were exposed to either short day length (10L:14D), long day length (14L:10D), or natural photoperiod in constant-environment rooms (25°C, 41% humidity; food and water ad libitum) for 8 wk in late summer, when males in the wild were spermatogenically active, and in mid-winter, when they were inactive. In neither experiment did prolonged exposure to short day length or naturally decreasing day length inhibit spermatogenic activity, and we conclude that the normal cessation of spermatogenesis that occurs in most male four-striped field mice in winter is not stimulated by day length alone.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Life histories of rodent species are characterized by extensive variation in the timing of reproductive activity [1, 2]. This variation, which may be between species or between populations of a single species, includes aseasonal, continuous reproduction at one extreme, and strongly seasonal reproduction with reproductive activity restricted to a short breeding season at the other. Between these extremes is a range of species in which the extent of seasonal inhibition of reproduction varies from slight to absolute [3]. The timing of reproduction in rodents is shaped by complex interactions between a range of environmental factors, such as climatic variability and food availability, that in turn are influenced by latitude; altitude and distance from the coast; a range of physiological factors such as longevity, diet, and body size; and other factors including predation pressure and phylogenetic and social constraints [4–8]. Studies of the control of reproduction have been concentrated at temperate latitudes in Europe and America where many species breed seasonally, for example the desert pocket mouse (Perognathus formosus) [9], the house mouse (Mus musculus) [10], and the deer mouse (Peromyscus maniculatus) [11]. Such seasonal reproduction is often controlled by a proximate cue like photoperiod but may also be triggered by rainfall, temperature, and/or secondary plant compounds [6, 11–19].

There are two principal reasons why individuals at lower latitudes are less likely to use photoperiod-cued seasonal reproduction. Firstly, as latitude decreases, the seasons become less marked, the climate less predictable, and the winter months not necessarily unsuitable for reproduction. And secondly, as latitude decreases, so does the extent to which day length changes—and below 10° the changes in day length may not be sufficient to act as a cue for reproduction [6, 20]. Despite there being good reason to expect that the control of reproduction will differ from temperate to tropical latitudes, there have been very few studies away from the temperate zone. The limited available data indicate that below 10° latitude, species are reproductively non-photoresponsive [21–25], and the single experimental study of the control of reproduction of rodents from sub-Saharan Africa indicates that photoperiod alone does not control reproduction in the seasonally breeding pouched mouse (Saccostomus campestris) [26].

The four-striped field mouse, Rhabdomys pumilio, is a small, diurnal rodent that has a mean body mass of 30–40 g [27–29]. It occurs through most of Africa, south of the Sahara [27, 29], and is mainly granivorous but also feeds on insects and green vegetable matter [18, 27]. Because of its diet, the four-striped field mouse is often attracted to cultivated lands, where it is known to cause considerable damage to young trees, especially to conifers in commercial plantations in South Africa [30]. The four-striped field mouse is a pioneer species and is one of the early colonizers of recently disturbed (burnt or cleared) areas [31].

Although the four-striped field mouse is a common species in southern Africa, there have been few published long-term investigations of its reproduction. The majority of studies have indicated that this species breeds seasonally, with inhibition of reproduction during the winter months of May to August (Pretoria: 26°S [32]; Grahamstown: 33°S [18, 19]; Cape Town: 34°S [27, 33]). The latter study, however, revealed that inhibition of reproduction in winter is not absolute. In their 5-yr study, the authors recorded three pregnant females in two of the winters; and of 427 males caught during the 5 yr, 7% were spermatogenically active during the winter. In Malawi, during a 19-mo study, Hanney [34] found that Rhabdomys pumilio bred during the summer months (October–May) with no evidence of reproduction during the winter. These studies indicate that seasonal reproduction is the most common reproductive strategy in the four-striped field mouse; however, in Botswana, pregnant females were recorded in January, February, June, and July, suggesting aseasonal reproduction [35]. In Kenya, the four-striped field mouse has opportunistic tendencies, producing large numbers of young in a short space of time when conditions are favorable [17].

The primary aim of the present program is to establish the role of environmental variables in controlling small mammal reproduction at low latitudes and in unpredictable environments. The four-striped field-mouse is used as a research model since it is common throughout southern Africa, breeds seasonally at high latitudes in the wild and readily in the laboratory [36], and is an agricultural pest when populations are large.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Animals

Four-striped field mice were trapped in March (late summer), May (early winter), and July (mid-winter) in Thomas Baines Nature Reserve in the Eastern Cape of South Africa (lat 33°18'S, long 26°32'E). In the laboratory, the mice were housed separately in standard rodent cages (36 x 24 x 18 cm) and supplied with shredded paper and sawdust for bedding. Food (consisting of mixed birdseed, rabbit pellets, and sunflower seeds) and water were provided ad libitum. In this species the testes move seasonally from an abdominal position in spermatogenically inactive males to scrotal in spermatogenically active males, and the reproductive condition (scrotal or nonscrotal) was assessed by observation.

To examine the effects of photoperiod on spermatogenesis, adult (> 25 g in mass), scrotal mice were maintained for 2 mo under either short-day conditions (10L:14D), long-day conditions (14L:10D), or natural photoperiod. The photoperiods used are the minimum and maximum experienced in the study area (Fig. 1A). The experiment ran for 2 mo because testicular regression occurs within 6 wk in the field (personal observation). During the experiments, the animals were caged separately in constant-environment rooms at a fixed temperature (25°C) and humidity (41 ± 5%). Food, water, and bedding were provided as described previously. The experiments were run during late summer (March/April), when males in the wild are approaching the end of reproductive activity, and in mid-winter (June/July), when they are typically spermatogenically inactive.



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  		FIG. 1. Hours of daylight (A) and a comparison of temperature (B) and rainfall (C) patterns for 1997 with mean values for the last 10 yr (1987–1996).

Experiment 1 (March/April)

Three groups, each consisting of five wild-caught scrotal males, were placed under either short-day, long-day, or decreasing natural photoperiod. Natural photoperiod during this experiment declined from 12.5 to 11 h. In this experiment, the timer for the lights in the short-day room failed and the results from this component could not be used.

Experiment 2 (June/July)

Two groups of nine F1 generation males, bred and maintained under natural photoperiod conditions with food and water ad libitum, were placed under either short- or long-day conditions. At the termination of this experiment (late July; mid-winter but increasing natural photoperiod), five males were caught in the wild to serve as a field control.

Throughout both experiments, males were weighed and their reproductive condition (scrotal, moving-scrotal, or nonscrotal) was recorded twice weekly. At the end of the 2 mo, the males were killed and weighed, and the testes, epididymides, and accessory glands (seminal vesicles and prostate gland) were removed. The reproductive organs were weighed (to 0.1 mg), fixed in Bouin's fixative, and prepared for light microscopy using standard techniques. Experiments were approved by the Rhodes University Ethical Standards Committee.

For each animal, 100 randomly selected seminiferous tubules from at least two sections through each testis were examined; the animals were classified as either spermatogenically inactive or in early or late spermatogenesis [26].

Twenty sections through the cauda epididymides were examined, and each animal was given a qualitative score depending on the amount of sperm present (0, no spermatozoa present; 1, cauda < half full of spermatozoa; 2, cauda half full of spermatozoa; 3, cauda > three quarters full of spermatozoa). The activity of the accessory glands was determined in a similar way, with the score being based on the amount of secretion present in 20 sections through the glands.

Mean masses were compared using repeated-measures ANOVA, ANOVA and Student's t-test, or the nonparametric equivalent, where applicable. There is a significant positive correlation between body mass and mass of the testes (p = 0.03, r = 0.38, r2 = 0.147), mass of epididymides (p = 0.02, r = 0.41, r2 = 0.17), and mass of the accessory glands (p = 0.0004, r = 0.591, r2 = 0.350); and we have compared both absolute and relative organ masses.

Climatic data came from a weather station located at Rhodes University, approximately 10 kilometers from the study site.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Experiment 1 (March/April)

Mean body mass at the end of the experiment was significantly greater than at the start for animals under both photoperiods (repeated-measures ANOVA, p < 0.01). At autopsy, there was no significant difference in the mean body mass or the mean absolute and relative masses of the testes, accessory glands, and epididymides of the animals from the long-day and natural photoperiods (Table 1). All the males, from both photoperiods, were scrotal and were spermatogenically active, with sperm stored in the caudae epididymides and secretion in the prostate gland and seminal vesicles (Table 2).


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  		TABLE 1. Mean body mass and relative masses of reproductive organs of male Rhabdomys pumilio, at dissection, from experiments 1 and 2.


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  		TABLE 2. Summary of the condition of the reproductive organs at dissection of male four-striped field mice from experiments 1 and 2.

Experiment 2 (June/July)

As in the first experiment, body mass of the animals from both short-day and long-day photoperiods increased through the experiment, and mean body mass was significantly greater at the end of the experimental period (p < 0.01). At autopsy there was no significant difference in the body mass of the animals from the two photoperiods (Table 1). Day length had no effect on either the relative or the absolute mass of the reproductive organs (Table 1), and all animals from the two photoperiods were scrotal and spermatogenically active (Table 2). The four-striped field mice collected from the wild at the end of the experiment were smaller than those that had been maintained in the laboratory (Table 1). The absolute masses of the testes and caudae epididymides were significantly lower in the animals from the wild, but, when these were converted to relative values, the differences were no longer significant (Table 1).

Field Observations and Climate

A single female collected in July was pregnant and gave birth in the laboratory on 3 August (4 days after capture).

The climate in the study area is strongly seasonal (Fig. 1), with a hot season from October to April (summer) and a cooler season from May to September (winter). The summer months are wetter and the winter months drier, but the seasonality of rainfall is masked by tremendous variability (Fig. 1C). Rainfall in early winter 1997 was much higher than usual (Fig. 1C). Day length ranges from 10L:14D (0700–1700 h, light) in June to 14L:10D (0500–1900 h, light) in December (Fig. 1A).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Seasonal reproduction, as has been reported for the four-striped field mouse, can be controlled in a number of ways. At high latitudes, where climatic seasonality is predictable, or in long-lived mammals, it is likely that photoperiod will be the principal proximate cue. By contrast, in short-lived species or in species from less predictable climates it is more likely that seasonality, if it occurs, will not be controlled by day length (see [6, 37, 38] for review). The major advantage of photoperiod is that it is the only entirely predictable environmental variable. However, utilizing photoperiod as a cue can result in an inflexible system that is less suited to an unpredictable environment and/or a species with a short life span.

In the present study, naturally decreasing and fixed short day lengths failed to inhibit spermatogenic activity at a time when males in the field would normally be undergoing testicular regression or be spermatogenically inactive. It appears therefore that the winter inhibition of reproduction previously reported for the four-striped field mouse is not controlled by photoperiod, and we suggest that reproduction is opportunistic (sensu Bronson [6]). Similarly, the pouched mouse (Saccostomus campestris), which occurs sympatrically with the four-striped field mouse, also breeds seasonally and is also reproductively non-photoresponsive [26].

In opportunistic species, reproduction is essentially continuous but is inhibited when there is an energy deficit. Opportunism can result in strictly seasonal reproduction if winters are always cold and food in short supply but will permit reproductive activity during an unusually warm, wet winter. This appears to be the case for the four-striped field mouse: while most studies show seasonal reproduction, the more complete long-term studies show occasional reproductive activity in winter ([27]; present study).

We suggest that the opportunistic strategy of the four-striped field mouse should be seen as an adaptation to the unpredictable nature of the climate, and particularly the rainfall, of the Eastern Cape of South Africa. It is worth noting that the Eastern Cape of South Africa is affected by El Nio Southern Oscillation events that add further unpredictability to the rainfall. It is likely that the above-average early-winter rains of 1997 resulted in an increase in food availability and thus allowed at least some members of the population to continue to reproduce through winter.

An opportunistic reproductive strategy will allow a species to respond rapidly to any change in food availability, such as occurs with the first rains after a grass fire; and it is thus not surprising that the four-striped field mouse is a pioneer species.

It is possible that the failure of short day length to inhibit spermatogenesis in the four-striped field mouse is a characteristic of the study population and not of the species. Indeed, Bronson [6] has observed that within certain populations some animals may be photoresponsive and others opportunistic, thus explaining how some animals can breed during winter and others not. If this were the case in the four-striped field mouse, then we should have caught members of both groups, and at least some of the animals would have responded to the experimental short photoperiods. This did not happen; all the animals responded in a similar way, and we believe that for the population we sampled, short day length does not inhibit spermatogenesis.

The available data for the four-striped field mouse suggest a latitudinal shift from continuous reproduction at tropical latitudes to seasonal reproduction at more temperate latitudes [17–19, 27, 32–35]. This could indicate a shift from reproductive non-photoresponsiveness at tropical latitudes to photoresponsiveness at more temperate latitudes as is seen, for example, in Peromyscus species in the Americas [6]. However, such a switch is unlikely in the four-striped field mouse, since our results indicate that individuals from more temperate latitudes are non-photoresponsive.

The normal cessation of spermatogenic activity that occurs in most male four-striped field mice in winter is inhibited under laboratory conditions of fixed ambient temperature and humidity and food and water ad libitum, irrespective of photoperiod. These results, combined with observations of small numbers of reproductively active animals in the field in winter, lead us to suggest that reproduction in the four-striped field mouse is opportunistic.


   ACKNOWLEDGMENTS
 
We would like to thank Claire Watcham for her assistance during the study and three anonymous referees who added to the clarity of the manuscript.


   FOOTNOTES
 
1 This research was funded by grants from the FRD and Rhodes University. Back

2 Correspondence. FAX: 46 6224377; zorb{at}warthog.ru.ac.za Back

Accepted: January 12, 1999.

Received: October 6, 1998.


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 ABSTRACT
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 RESULTS
 DISCUSSION
 REFERENCES
 

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