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Biology of Reproduction 66, 415-420 (2002)
© 2002 Society for the Study of Reproduction, Inc.

Regular Article

Long-Day Inhibition of Reproduction and Circadian Photogonadosensitivity in Zembra Island Wild Rabbits (Oryctolagus cuniculus)

M.M. Ben Saada, and D.L. Maurel1,b

a Laboratoire de Physiologie Animale, Faculté des Sciences de Tunis, Campus Universitaire, 1060 Tunis, Tunisia b Pathologie de l'Oreille interne et Réhabilitation, EPI 9902 INSERM, Faculté de Médecine Nord, 13916 Marseille cedex 20, France


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
We investigated the effects of photoperiod on testicular activity in wild rabbits (Oryctolagus cuniculus) captured on Zembra Island (North Tunisia) and maintained in experimental photoperiodic conditions. Sexually inactive animals were subjected to alternate 3-mo periods of short days (8L:16D) and long days (16L:8D) for 1 yr. Testicular activity increased significantly and then decreased to levels equivalent to or lower than those measured during sexual quiescence after 1 mo of 8L:16D or 16L:8D, respectively. Eight groups of sexually active animals were also exposed to 8L:16D for 60 days. The light phase was divided into two photofractions (7.5 and 0.5 h). The short photofraction interrupted the dark phase 9.5–18.5 h after the beginning of the main photofraction. Testicular activity was inhibited if the short photofraction interrupted the dark phase 12.5 h or more after the beginning of the main photofraction. These results clearly confirm that photoperiod affects reproduction in this species: Short days stimulate reproduction, whereas long days inhibit it. The asymmetric pattern of skeleton photoperiods used demonstrated the existence of a circadian rhythm for photogonadosensitivity, with the photosensitive phase beginning 12.5 h after dawn. In this species, photoperiod length controls both the beginning and the end of the reproductive period. These results differ from those obtained with continental populations of wild rabbits, in which reproduction is inhibited by short day length. This difference may reflect genetic drift linked to the geographic isolation of this population, which is known to have been present on this small island for more than 2000 yr.

environment, male sexual function, seasonal reproduction, steroid hormones, testis, testosterone


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In most mammals living in temperate climates, reproduction follows a seasonal pattern that is often under photoperiodic control. Such patterns have evolved so that animals give birth during periods when environmental conditions are favorable, maximizing the chances that the young will survive. One of the most reliable seasonal predictors appears to be the photoperiod [1, 2]. Depending on the species, photoperiod may either trigger onset of the reproductive period (a stimulating effect) or initiate gonadal regression (an inhibiting effect). In long-day breeding species, the seasonal increase in sexual activity occurs when the amount of daylight increases, and in short-day breeding species, the reproductive season is triggered by the shortening of day length. Melatonin, a 5-methoxyindole synthesized by the pineal gland, plays a major role in photoperiod-mediated control of reproduction in mammals with seasonal breeding patterns determined by day length in their natural environment, and the circadian pattern of melatonin secretion constitutes an endocrine message that provides information regarding the photoperiod [3–6].

In a previous study involving a population of wild rabbits (Oryctolagus cuniculus) on Zembra Island, we showed that testicular activity begins in late autumn (October–November), in short-day conditions [7], and that this seasonal increase in testicular activity is prevented by superior cervical ganglionectomy [8]. After ganglionectomy, no seasonal increase in testicular activity or endogenous circannual rhythm of reproductive activity was observed in this species during the following year. Subcutaneous melatonin implantation in ganglionectomized animals led to the reactivation of testicular activity, demonstrating the stimulating role of the pineal hormone on the gonads; similar melatonin implants in intact animals prolonged the reproductive period by 2 mo [9]. Although the role of short days (and of melatonin) in the renewal of reproductive activity has been clearly demonstrated in this species, the factor that is responsible for determining the end of the reproductive period is, to our knowledge, unknown. We investigated whether long days were involved in the control of testicular regression in this population of short-day breeding rabbits by studying the effects of alternate 3-mo periods of short (8L:16D) and long (16L:8D) days on testicular activity for 1 yr. We also studied the effect of an asymmetric skeleton photoperiod [10] (7.5 + 0.5 h) on testicular regression in sexually active males. Testicular activity was assessed by determining testis volume and plasma testosterone concentration.


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

The rabbits (Oryctolagus cuniculus) were trapped on Zembra Island (30°50'N, 10°14'E) in the north of Tunisia in July (experiment 1) and early September (experiment 2) during the sexual resting period (May–September). All animals used in this study were adult males in good condition. The experiments were performed in accordance with European Community Council Directive 86/609/EEC. Once caught, animals were transferred to the laboratory, where they were placed in individual cages. They were fed an appropriate daily diet (rabbit chow; SNA, Tunis, Tunisia) and given water ad libitum.

Experimental Schedule

Experiment 1 Eight adult male rabbits were randomly assigned to two treatment groups of four animals each: natural photoperiodic conditions, and experimental photoperiodic conditions. Both groups were kept in natural photoperiodic conditions for 1 mo, then (from September) the experimental animals were subjected to alternate 3-mo periods of short days (8L:16D) and long days (16L:8D) for a total of 1 yr. The two groups were studied over 13 mo.

Experiment 2 Forty adult male rabbits were randomly assigned to eight treatment groups of five animals each. The eight groups were housed in controlled-photoperiod rooms with a gonadostimulating, 8L:16D regime for 2 mo before the start of the experiment in November, when animals are sexually active. Group 1 was maintained in 8L:16D conditions. Groups 2–8 were also given light for 8 h, but the light phase was divided into two photofractions: a main photofraction of 7.5 h, and a short photofraction of 0.5 h. The short photofraction interrupted the dark phase at various intervals (9.5, 10.5, 11.5, 12.5, 14.5, 16.5, and 18.5 h after the beginning of the main photofraction for groups 2–8, respectively). Considering the annual variations in day length at Tunis (9 h 40 min to 14 h 43 min), the photoperiodic protocol used for groups 1 through 4 corresponded to the natural photoperiod occurring during the period of sexual activity (autumn and winter), and the photoperiodic protocol used in group 6 corresponded to the natural photoperiod occurring during the period of sexual rest (late spring to early summer). The photoperiod used for group 5 corresponded to that of the spring equinox (end of March), when sexual activity begins to taper off. The durations of the photoperiods used for groups 7 and 8 differed from the natural day length and corresponded to group controls for very long photoperiods (Fig. 1). For all groups, the duration of the experiment was 60 days.



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  		FIG. 1. Experimental schedule of the asymmetric 8L:16D photoperiods to which the eight groups of rabbits (Oryctolagus cuniculus) were exposed. The control group (G1) was subjected to the normal 8L:16D regime. For groups 2–8 (G2-G8), the light phase consisted of a main photofraction of 7.5 h and a secondary photofraction of 0.5 h interrupting the 16-h dark period at various times after the start of the main photofraction (G2: 9.5 h; G3: 10.5 h; G4: 11.5 h; G5: 12.5 h; G6: 14.5 h; G7: 16.5 h; G8: 18.5 h). The timing of the secondary photofraction was related to the annual variations of light and dark phases at the latitude of Zembra Island (lower part of the figure), with a seasonal minimum of 9 h 40 min of light (winter solstice, 21 December) and a maximum of 14 h 43 min (summer solstice, 21 June)

Measurement of Testicular Activity

To evaluate testicular activity, we measured two variables: testis volume (cm3), indicating spermatogenetic activity; and plasma testosterone level (ng/ml), indicating endocrine activity. The dimensions of the testis—length (L), width (W), and thickness (T)—were measured to the nearest 0.1 mm with calipers, through the scrotum, and the formula V = 4/3 x {pi} x L/2 x W/2 x T/2 was used to calculate testis volume.

The testes were measured and blood from the ear marginal vein collected once per month, between 0900 and 1100 h, for all animals during the 13 mo of experiment 1 and at the start (Day 0) and end (Day 60) of experiment 2. The blood was centrifuged for 15 min at 1500 x g, and the plasma was stored at -20°C until assay.

Plasma testosterone was determined by radioimmunoassay using a commercial kit (Spectria Direct Testosterone; Orion, Espoo, Finland). Each plasma sample (50 µl) was assayed in duplicate. Sensitivity, defined as the smallest quantity of hormone detectable, was 4 pg/tube. The intra- and interassay coefficients of variation were 6.5% (n = 15) and 7.8% (n = 5), respectively.

Statistical Analysis

Monthly values are presented as means ± SEM. For experiment 1, we checked that the data were normally distributed. If this was not the case, the data were normalized by Ln transformation (for plasma testosterone concentration). Data were subsequently analyzed by one-way ANOVA and pairwise multiple comparison by Student-Newman-Keuls test (SigmaStat; SPSS Science Software GmBH, Erkrath, Germany). For experiment 2, the initial and final states of the various groups were compared by two-way ANOVA with repeated measurements followed by a post-hoc Fisher least significant difference test. Differences between monthly values for the same group or between groups at a given time point were considered to be statistically significant at P < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Experiment 1: Testicular Inhibition by Long Days

The control animals (Fig. 2, A and B) displayed no testicular activity at the start of the experiment (September). The first signs of testicular activity were detected in November–December. Plasma testosterone levels peaked in January (9.42 ± 1.22 ng/ml), decreased drastically in February, and reached levels indicating inactivity in March (2.07 ± 0.67 ng/ml). Testis volume was high from December to March (maximal values in January and February: 2.78 ± 0.37 and 3.12 ± 0.52 cm3, respectively) and reached its minimal level in May (0.73 ± 0.13 cm3).



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  		FIG. 2. Effects of the alternate short-day, long-day regime on the testicular activity of wild rabbits from Zembra Island (ExpC). A control group of animals (NC) was concomitantly subjected to natural conditions of photoperiod and temperature

Testicular activity began earlier in the experimental animals than in the controls. After 1 mo of short-photoperiod conditions (8L:16D), testis volume and plasma testosterone levels were significantly higher than those measured in the control group or at the beginning of the short-photoperiod treatment. At the end of the 3-mo period of short days, plasma testosterone levels peaked (9.12 ± 1.43 ng/ml) and were similar to those measured in controls (January peak: 9.42 ± 1.22 ng/ml). After 1 mo of long days (16L:8D), testis volume and plasma testosterone levels had decreased dramatically, such that plasma testosterone levels were equivalent to or lower (0.32 ± 0.07 ng/ml) than those measured during the period of sexual rest in control animals (i.e., May: 1.26 ± 0.45 ng/ml). These values remained low until the end of the long-day regime. Similar profiles were obtained for plasma testosterone concentration and testis volume if the animals were subjected to the same alternate-photoperiod regimen for a second time, with a significant increase after 1 mo of short days and a peak in plasma testosterone concentration at the end of the 3-mo period of short days (8.56 ± 1.26 ng/ml), followed by a drastic decrease after 1 mo of long days (0.37 ± 0.13 ng/ml).

Experiment 2: Circadian Variation in Photogonadosensitivity

At the start of experiment 2, all animals were sexually active, as shown by the mean testis volume of 1.93 ± 0.06 cm3 (range: 1.25–2.7 cm3; no difference between groups, P > 0.05) and plasma testosterone concentration of 6.31 ± 0.15 ng/ml (range: 5.10–8.95 ng/ml; no difference between groups, P > 0.05, n = 40). For testosterone concentration, a group effect (F = 22.07, P < 0.001), a treatment effect (F = 78.43, P < 0.001), and a combined group-treatment effect (F = 25.10, P < 0.001) were observed. Similarly, for testis volume, a group effect (F = 10.97, P < 0.001), a treatment effect (F = 45.25, P < 0.001), and a combined group-treatment effect (F = 10.98, P < 0.001) were observed. At the end of the experiment, testis volume (Fig. 3A) and testosterone concentration (Fig. 3B) remained unchanged for groups 1–4, in which the 0.5-h photofraction was given directly after the main photofraction (group 1) or no more than 12 h after the beginning of the main photofraction (groups 2–4), which corresponds to the natural duration of short days at this latitude. Conversely, in groups 5–8, a drastic reduction in testicular activity was observed (group 5: P = 0.001; groups 6–8: P < 0.001), although this was less pronounced in group 5. The mean values for groups 6–8 were 1.18 ± 0.06 cm3 (testis volume) and 0.58 ± 0.05 ng/ml (plasma testosterone concentration) at the end of the experiment. This corresponds to a decrease of 70% and 80% for testis volume and plasma testosterone concentration, respectively. These values were identical to those measured in control animals (Fig. 2) during the quiescent period. Testicular activity was decreased twice as strongly in groups 6–8 as in group 5 (i.e., 37% for testis volume and 54% for plasma testosterone concentration).



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  		FIG. 3. Testis volumes (cm3; A) and plasma testosterone concentration (ng/ml; B) between the beginning and the end of the 60-day experiment in the control group (G1; 8L:16D) and the seven experimental groups subjected to an asymmetric photoperiod (G2–8; details in Fig. 1). Asterisks indicate a statistically significant difference (P < 0.05) in the same group between final and initial values (A) or between G2–G8 and G1 (B)


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The results of this study confirm previous reports that the testicular activity of wild rabbits from Zembra Island reared in natural temperature and photoperiodic conditions is seasonal, increasing in autumn [7, 9]. We have previously shown that experimental exposure to short days (8L:16D) at the beginning of summer reactivates gonadal activity in this species [8], that s.c. melatonin implants in ganglionectomized animals renew testicular activity [9], and that, after bilateral superior cervical ganglionectomy, the natural short days that occur after the autumn equinox cannot stimulate gonadal activity. As observed in this species after optical nerve section (NOx) [11], testicular function did not increase, even 13 mo after bilateral ablation of the superior cervical ganglion (SCGx). The lack of a testis cycle in these constant-photoperiod conditions (NOx) or if the seasonal melatonin signal is abolished (SCGx) after more than 1 yr suggests that, in this species, the reproductive seasonal rhythm is not self-sustained. The lack of testis stimulation and the reactivation of gonad function following s.c. melatonin implantation in ganglionectomized rabbits and the longer duration of testicular activity in intact animals bearing melatonin implants [9] in another short-day breeding mammal, the mink [12, 13], confirm that the pineal gland and melatonin are involved in the seasonal activation of reproduction in short-day breeding species. Indeed, our results confirm that experimental short days renew testicular activity, and that experimental long days drastically inhibit testicular exocrine and endocrine activity. Thus, in this species, both parts of the sexual cycle (stimulation and inhibition) are controlled by the photoperiod.

The results of experiment 2, showing that plasma testosterone concentration and testis volume depend on the timing of the photofractions, identify a daily phase during which light has an inhibitory effect on testis function in our experimental conditions. This phase began 12 h after the start of the main photofraction. The photoresponse observed in the Zembra Island rabbit is similar to that described in another short-day breeding mammal, the mink [14], and in a semidesert rodent from Africa, Arvicanthis niloticus [15]. The experiments conducted on the mink started during the period of testicular inactivity and demonstrated that photoinhibition prevents the induction of testicular activity [14, 16]. However, to our knowledge, no experiments have been carried out in the mink to determine whether long days inhibit testicular activity in sexually active animals. The experiments involving A. niloticus were performed with sexually active animals [15, 17] in conditions similar to those used in this study. However, the phase of potential inhibition occurred 11.5 and 12.25 h after the start of the main photofraction for animals originating from Burkina Faso and Mali, respectively, showing a clear geographic difference. Long days (>12.5 h) were shown to inhibit testicular activity in these semidesert rodents. However, this species starts to breed when day length is just 11.0 h, in temperatures of between 20 and 25°C, and in humid conditions. If temperatures are high (30–35°C), significantly lower levels of sexual reactivation are observed, even if the day length is short (11 h) and the conditions humid [18], showing that other environmental factors, such as temperature and humidity, have a modulating effect. Given annual variations in day length at the latitude of Zembra Island (approximately the same as that of Tunis), testicular activity is inhibited if day length exceeds 12.5 h (group 5), corresponding to the first few days after the spring equinox (end of March), but regression is only complete if day length is 13.5 h or more (groups 6–8).

Studies conducted in England and in France have characterized the female and male reproductive cycles of the wild European rabbit [19–22]. Testicular activity is maximal from January to June–July. It then decreases in summer, and a period of rest occurs between October and December. Gravid females are observed only between February and August. Thus, the wild European rabbit appears to be a long-day breeder, the sexual activity of which is inhibited by short days. This was demonstrated experimentally by Boyd [21], who showed that the transfer from long (16L:8D) to short (8L:16D) days or the insertion of s.c. melatonin implants in rabbits maintained in long-day conditions caused testicular regression. We obtained the opposite result, showing that the wild rabbit population of Zembra Island is a short-day breeder, in which reproductive activation is driven by short days and melatonin and is inhibited by long days.

The existence of intraspecific geographic differences in photoperiodic control of the sexual cycle has been demonstrated in small populations of various rodents, such as Peromyscus leucopus [23–25] and P. maniculatus [26] in North America and A. niloticus in West Africa [15]. Within a given population, individuals display a spectrum of responses, from a full response to a total lack of response, to the reproductive effects of photoperiod (Microtus ochrogaster [27], M. agrestis [28], P. leucopus [29], and M. pennsylvanicus [30]). In the hamster (Phodopus sungorus), a laboratory mammal, artificially selected genotypes that are probably not produced by natural selection showed genetic variation in short-day responsiveness [31, 32]. In this species, such genetic variation may be related to photoperiodic history [32]. Although these well-studied species (hamsters and rodents) can vary from short-day responsive to short-day unresponsive, they have not been shown to be subject to inverse regulation (long days vs. short days) like the rabbit (O. cuniculus). In larger mammals, the only description of this type of inverse regulation, to our knowledge, is in a population of Ouled-Djellal rams living in the southern part of Algeria, near the Sahara desert [33, 34]. In contrast, in rams from the Northern hemisphere, mainly North America, France, and England [35–40], breeding activity peaks when day length decreases.

The insularity (isolation syndrome [41]) of this rabbit population, known to be isolated on Zembra Island for more than 2000 yr, may account for this pattern of photogonadoregulation [9] being opposite to that observed in continental populations, and it may illustrate genetic adaptation. Winter reproduction (December–January) leads to births in January–February. The young suckle for 1 mo and then are weaned in March, the most favorable period in terms of temperature (mild) and natural feeding (abundant herbaceous plants after the winter rains). These good natural conditions enable the young to grow and to gain weight quickly. This increases the chances that the young will resist the harsh conditions of the summer period (May–September), which is characterized by high temperatures, no rain, and very scarce vegetation. Reproduction in spring or early summer, leading to the birth and weaning of young during the summer months (as with continental populations in Europe) would almost certainly be unsuccessful due to the extremely unfavorable environmental conditions in summer and the lack of underground burrows, although the soil of Zembra Island is suitable for burrowing. As discussed previously [9], the wild rabbits of Zembra Island do not excavate, and this specific behavior may have played a role in the death of the young of a female that gave birth late in the season.

No precise information is available concerning the first populations of rabbits to colonize this island more than 2000 yr ago. They were probably introduced by Greek, Phoenician, and then Roman fishermen with a view to ensuring the food supply. In such a rabbit population, returned to the wild and probably reproducing in the summer (as observed in continental populations), only those individuals with winter-breeding behavior, which would have rendered them marginal in the normal range of the population, would have been able to ensure the survival of the species. Evidence that this may indeed have occurred is provided by reports of full sexual activity during winter in some males of a population of rabbits in France [20]. The response to photoperiod (inhibition by long days) of the Zembra Island rabbit may result from an endogenous circadian rhythm in photogonadosensitivity caused by the light-dark cycle. Whether the observed long-day inhibition results from a decrease in melatonin concentration when nights become shorter or is linked to a more complex mechanism, such as thyroid-testicular interactions involving another external factor (e.g., temperature), is unclear. We are currently studying interactions between thyroid activity and testicular cycle in response to variations in temperature and photoperiodic conditions.


   FOOTNOTES
 
First decision: 16 July 2001.

1 Correspondence: Daniel Maurel, Pathologie de l'Oreille interne et Réhabilitation, EPI 9902 INSERM, Faculté de Médecine Nord, Boulevard Pierre-Dramard, 13916 Marseille cedex 20, France. FAX: 04 91 69 87 31; maurel.d{at}jean-roche.univ-mrs.fr Back

Accepted: September 24, 2001.

Received: June 18, 2001.


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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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M.M. Ben Saad and D.L. Maurel
Reciprocal Interaction Between Seasonal Testis and Thyroid Activity in Zembra Island Wild Rabbits (Oryctolagus cuniculus): Effects of Castration, Thyroidectomy, Temperature, and Photoperiod
Biol Reprod, April 1, 2004; 70(4): 1001 - 1009.
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