CITE THIS ARTICLE AS “IN PRESS” Basic and Applied Herpetology 00 (0000) 000-000

Reproductive cycle of male wall , vaucheri (Reptilia: Sauria: ), in Djurdjura, Northern Algeria

Rabah Mamou1*, Elara Moudilou2, Mansour Amroun1, Jean-Marie Exbrayat2

1 Laboratoire d’écologie des vertébrés, University Mouloud MAMMERI of Tizi Ouzou, Algeria. 2 University of Lyon, UMRS 449, General biology – Reproduction and comparative development, Lyon Catholic University, EPHE/PSL, 10 place des Archives, 69288 Lyon Cedex 02, France.

*Correspondence: E-mail: [email protected]

Received: 15 February 2017; returned for review: 5 April 2017; accepted 4 September 2017.

The reproductive cycle of male wall lizard Podarcis vaucheri (Boulenger, 1905) living in Djurdjura Mountain, was analyzed from April until October 2014. Its seasonal mixed-type cycle was charac- terized by three phases: sexual activity, quiescence and recrudescence. After the emergence of liz- ards from hibernation, an intense sexual activity was observed in spring (April, May, and June), at which the testicular weight and seminiferous tubules diameter reached their maximal values. At this period, spermiogenesis was also maximal and the spermiation allowed the release of a large quantity of spermatozoa in both the seminiferous tubules and epididymis lumen. In July, a short sexual resting period followed, during which the testes mass and seminiferous tubules diameter decreased. Spermatogonia and some primary spermatocytes were observed against the wall of seminiferous tubules. The recrudescence period (August, September and October) was character- ized by a progressive increase of the testis weight and seminiferous tubules diameter. Spermato- cytogenesis began in August, and spermiogenesis occurred in September and October, before the diapause period. However, the presence of spermatozoids was not signaled in the epididymis lu- men. Field observations and microscopic evidence of testis showed that both sexes reproduced synchronously during spring and early summer.

Key words: Algeria; Djurdjura; Lizard; Podarcis vaucheri; reproductive cycle; spermatogenesis.

Reproduction imposes high-energy ard’s biology (James & Shine, 1985). For requirements, illustrated by a large diver- that, the reproduction occurs when the sity in terms of resource acquisition and environment is the most favorable to off- allocation strategies (Jönsson, 1997). Sea- spring survival and when parents can sonal breeding represents a valuable strat- physiologically sustain reproduction with egy in order to use this energy economical- the lowest cost (Whittier & Crews, 1987; ly, but the reproductive timing becomes Pianka & Vitt, 2003). one of the most critical issues in the liz- Timing of reproductive activity is

DOI: http://dx.doi.org/10.11160/bah.77 Supplementary material available online MAMOU ET AL. widely variable in (Manríquez- Ikeuchi, 2004). Being partly predetermined Morán et al., 2005; Carretero, 2006; (Angelini et al., 1976), it is also expected Villagrán-Santa Cruz et al., 2009; Grib- that these mechanism are subject to some bins, 2011): in temperate-zones, breeding kind of phylogenetic constrains (Dunham takes place in spring and early summer, & Miles, 1985; Carretero, 2006), which with the reproductive season being longer can limit the observed environmental and in coastal than in continental populations geographic variability. On the other hand, (Carretero & Llorente, 1995,1997; Galán, the relationships between reproductive 1997; Carretero et al., 2006a, Al-Amri et cycles and environmental variables sug- al., 2012), while in cold and high-altitude gest that the endogenous mechanisms can environments, mating occurs later in the plastically respond to climatic compo- season and lizards exhibit a short breeding nents, such as temperature (Licht, period (Saint-Girons & Duguy, 1970; Hra- 1971,1973; Aldridge, 1975; Angelini et al., oui-Bloquet, 1985; Hraoui-Bloquet & 1976; Marion, 1982; Flemming, 1993; Car- Bloquet, 1988; Braña et al., 1990; Olsson & retero, 2006; Abu-Zinadah, 2008), precipi- Shine, 1999; Roig et al., 2000; Arribas & tation (Jenssen & Nunez, 1994), photoperi- Galán, 2005). Further, in desert environ- od (Licht, 1971,1973; Dunham & Miles, ments reproduction can be postponed as 1985; Flemming, 1993; Carretero, 2006), well as anticipated compared to temperate or other environmental features, like food zones (Hammouche & Gernigon- availability (Lofts, 1978; Marion, 1982; Spychalowicz, 1996; Hammouche et al., Colli et al., 2003; Domínguez et al., 2010). 2007; Goldberg, 2013), and can continue The seasonal testicular cycle in lizards until autumn (Goldberg, 2013). Lastly, it is was described in several (Al-Amri in tropical areas that lizards exhibit the et al., 2013). Specifically, for temperate re- highest variability of reproductive gions three spermatogenic cycles were patterns, ranging from continuous to sea- described: i) the vernal or prenuptial type, sonal reproduction (Fitch, 1970; James & where spermatogenesis occurs during Shine, 1985; Jenssen & Nunez, 1994; Pi- spring, immediately before or even during anka & Vitt, 2003; Huang, 2010; Méndez- breeding (Licht et al., 1969; Saint-Girons, de la Cruz et al., 2013). 1982; Carretero, 2006); ii) the postnuptial Besides the environmental conditions, type, where spermatogenesis is held dur- several studies showed reproductive cy- ing summer of the previous year (Saint- cles to be influenced also by the interaction Girons, 1982; Carretero, 2006; Hraoui- between endogenous and exogenous fac- Bloquet et al., 2007); iii) an finally the tors (Licht et al., 1969; Licht, 1972; Ange- mixed type, where spermatogenesis be- lini et al., 1976; Lofts, 1978; Marion, 1982; gins at the end of summer and is interrupt- Jenssen & Nunez, 1994; Carretero, 2006). ed in winter (Licht et al., 1969; Saint- On one hand, indeed, the gonadal and Girons, 1982; Carretero, 2006). However, hormonal activity can be considered the Saint-Girons (1982) recognized two sub- main endogenous mechanisms controlling types of this cycle. The first sub-type corre- reproductive cycles (Díaz et al., 1994; sponds to the classical definition, with

2 SPERMATOGENESIS CYCLE OF THE WALL LIZARD OF DJURDJURA spermiogenesis extending until spring of Moreira et al., 2014), none of them has the following season. While in the second focused on describing the reproductive sub-type, there are two periods of spermi- cycle of this variable species. ogenesis, spermatozoa are already pro- The aim of the present work was to duced in autumn of the previous season describe the spermatogenic cycle of male and continues in spring after hibernation. wall lizards Podarcis vaucheri based on the Whatever the cycle, in most cases spermat- histological analysis of testis, in order to ogenesis is synchronized with vitellogene- provide some preliminary information sis and ovulation in females (Pianka & about its reproductive strategy. Vitt, 2003; Carretero, 2006). Material and Methods Lizards of the genus Podarcis (Wagler 1830) represent a group that has evolved Site of study and diversified in the Mediterranean Basin Tala Guilef is located in the western (Arnold et al., 2007). An exemplary case is part of the northern slope of the Djurdjura that of the complex, Mountain (Djurdjura National Park), Ka- which is among the most studied Europe- bylie, Algeria. It is located approximately an , and is characterized by a high 140 km southeast of Algiers and 45 km genetic diversity (Kaliontzopoulou et al., south west of Tizi Ouzou (36°39’ N, 4°01’ 2011). The inclusion of genetic sequences E). The region is characterized by a moun- from North African specimens has al- tain climate influenced by the Mediterra- lowed the separation of P. vaucheri from nean Sea, and belongs to the humid cli- the hispanicus complex, and elevating it to mate scene (Hamdine et al., 1993). the species rank (Oliverio et al., 2000; Bus- The specimens were collected in a ack et al., 2005). In addition, morphologi- rocky environment particularly attractive cal and phylogenetic studies of Iberian and for this species, characterized by the pres- North African populations (Oliverio et al., ence of stones and rocks from the Haïzer 2000; Busack et al., 2005; Pinho et al., massif and bushy vegetation including: 2006,2007; Larbes et al., 2007; Lima et al., Crataegus monogyna, Crataegus laciniata, 2009; Renoult et al., 2010; Kaliontzopou- Rubus ulmifolius, Rosa canina, Rosa sicula, lou et al., 2011,2012) have shown the oc- Prunus prostrata and Berberis hispanica. In currence of several evolutionary lineages grass stratum, we essentially found: Anthe- suggesting that Podarcis vaucheri can be mis kabilica, Artemisia absintium, Astragalus considered a species complex. Further- armatus, Eryngium tricuspedatum, Euphorbia more, very few information is available, luteola and Ferula communis. especially on the ecology and physiology of this species. Notably, even if some pre- Data analysis vious studies have provided data on Adult males of P. vaucheri were collect- trophic ecology (Carretero et al., 2006b; ed monthly (between the tenth and the Mamou et al., 2016), thermal biology twenty-fifth day of each month; three indi- (Veríssimo & Carretero, 2009), and para- viduals/month), from April until October sitology (Carretero et al., 2011; Damas- 2014. The snout-vent length (SVL) of each

3 MAMOU ET AL. individual was measured using a digital Results caliper (± 0.01 mm). After dissection, the Mean snout-vent length (SVL) of liz- left testes were removed, weighted with a ards was 54.73 ± 0.50 mm, ranging be- digital balance (± 0.0001 g), and fixed tween 50.85 and 58.74 mm. A positive cor- with buffered formalin for 24 hours, and relation was found between testicular then preserved in ethanol 70°. The tissues weight and body size (SVL) (r = 0.44, P = were dehydrated in a graded series of 0.047). The weight of testis varied ethanol, cleared in butanol prior to be significantly throughout the months infiltrated and embedded in paraffin. 5 (ANCOVA F(6,13) = 44.51, P < 0.0001), and µm sections were stained with hematoxy- the spermatogenesis cycle of P. vaucheri lin-eosin, following standard histological might be divided into three main phases protocols. (Fig. 1): i) the phase of sexual activity Spermatogenic activity was assessed (April, May, June), which was character- qualitatively by determining the various ized by the highest weight; a short period stages of germ cells. The presence of sper- of regression and a sexual quiescence matozoa and secretions in the epididymis (July), during which the testis weight de- lumen were also noted. For a quantitative creased; a recrudescence phase (August, characterization of testis activity, three September, October), where the testicular measures were taken: the (i) number and weight started to increase (August), reach- (ii) diameter of seminiferous tubes, and ing its maximum in October, just before (iii) epididymis epithelium thickness. the period of hibernation (November – These measures were repeated on three March). randomly selected testis sections for each individual (Table S1). Sections of each testis were examined and photographed using a Nikon Eclipse E400 light microscope, equipped with a Nikon digital DXM1200 camera coupled with a picture analyzer Nis-Element BR 3.1(Lucia software). For the data analysis, the mean value of each histological parameter among the three sections of each individual was con- sidered. All parameters were Log trans- formed, and comparisons between the Figure 1: Monthly variation of mean weight different measurements were performed testes in P. vaucheri. with ANCOVA, using the logarithm of The average number of seminiferous SVL as a covariate. Further, to investigate tubules by section oscillated between 45 the influence of body size in the gonadal and 55 (Fig. 2A), and did not vary along development, we used a Pearson correla- the season (F(6,13) = 0.6, P = 0.726). On the tion between SVL and testis weight. contrary, the mean diameter of the semi-

4 SPERMATOGENESIS CYCLE OF THE WALL LIZARD OF DJURDJURA

Figure 2: Monthly variation of the (A) mean number and (B) the diameter of the seminiferous tubules in P. vaucheri. niferous tubules showed a clear monthly the emergence of lizards in spring (sexual variation (F(6,13) = 9.18, P = 0.005; Fig. 2B), activity), the spermiogenesis was maximal peaking during the breeding season(April- and persisted until June, so, all sperm cells June). The sexual resting period was char- categories were observed (Fig. 4A), with a acterized by a maximal regression of the decrease of spermatocytes number. The seminiferous tubules diameter with an spermiation allowed the release of a large absence of lumen. During the period of quantity of spermatozoa in the lumen of recrudescence this parameter increased the seminiferous tubules and epididymis. progressively again, with the lumen re- Moreover, the morpho-functional charac- maining absent in August (Fig. 4E). The teristics of the epididymis have changed; evolution of the diameter of seminiferous the epithelial cells became secreting and tubules corresponded to the resumption of take a prismatic shape (Fig. 4B). testicular activity interrupted in Novem- ber by the temperature decrease, and fol- lowed by the beginning of hibernation. The thickness of the epididymis epithe- lium showed a significant monthly varia- tions (F(6,13) = 32.23, P < 0.001; Fig. 3). Dur- ing the phase of sexual activity this param- eter was at maximum, while a sudden re- duction of the height was observed in July, persisting until October. The examination of histological sec- Figure 3: Monthly variation of the epididymis tions revealed some variations of the epithelium height in P. vaucheri. different categories of germinal cells dur- ing the reproductive cycle (Fig. 4). After In July, at sexual rest, the seminiferous

5 MAMOU ET AL. tubules contained spermatogonia and of spermatogonia. Testicular recrudes- some primary spermatocytes (Fig. 4C). In cence started early in late summer (in Au- August, at the beginning of the recrudes- gust) and some young spermatides were cence period, the seminiferous tubules already observable. Testis weight in- showed a lot of primary and secondary creased progressively until the onset of spermatocytes, and some young sperma- hibernation; and that is accompanied with tids (Fig. 4E). In September and October a development of the seminiferous tubules spermiogenesis occurred, and a large corresponding to the spermatogenic activi- number of spermatid and spermatozoa ty. These observations are in agreement were found in the seminiferous tubules with those of mountains populations, such lumen (Fig. 4G). as Phoenicolacerta laevis (Mahrouka- In spite of an active spermiogenesis in Sannine Mount in Lebanon; Hraoui- autumn accompanied with the presence of Bloquet, 1985; Hraoui-Bloquet & mature spermatozoids in the lumen of the Bloquet, 1988), P. muralis (Orédon Biolog- seminiferous tubules, the epididymis lu- ic Station of High Pyrenees in France; men remained empty (Fig. 4H). Saint-Girons & Duguy, 1970), and Iberol- acerta monticola (high and low altitudes in Discussion Asturias in northern Spain; Braña et al., The spermatogenic cycle of Podarcis 1990). However, a very early stop of the vaucheri is of the “mixed-type”, in agree- spermatogenesis was reported at the end ment with what is the dominant pattern in of May in Phoenicolacerta laevis (Hraoui- temperate lizards (Licht et al., 1969; Saint- Bloquet, 1985; Hraoui-Bloquet & Girons, 1982; Carretero, 2006), especially Bloquet, 1988), which is not the case in P. those belonging to the genera Lacerta s.l. vaucheri. and Podarcis (Saint-Girons & Duguy, 1970; In addition to the obvious spring testic- Angelini et al., 1979; Hraoui-Bloquet, ular activity, another active spermiogene- 1985; Hraoui-Bloquet & Bloquet, 1988; sis was also found in September and Octo- Braña et al., 1990; Castilla & Bauwens, ber. Finally, this defines two periods of 1990; Galán, 1996; Amat et al., 2000; Roig spermiogenesis, corresponding to the sec- et al., 2000; Carretero et al., 2006a). Males ond sub-type of the mixed cycle (Saint- of P. vaucheri exhibited an intense sexual Girons, 1982). Similar results were already activity in April after the hibernation observed in several Mediterranean lacer- phase, followed by an interruption of the tids such as Podarcis muralis (Saint-Girons spermatogenesis in June. Then, a short & Duguy, 1970), Podarcis siculus campestris sexual resting phase was observed during (Angelini et al., 1979), Zootoca vivipara the hot period of the year, specifically in (Roig et al., 2000), Podarcis bocagei July and at the beginning of August. This (Carretero et al., 2006a), Iberolacerta monti- period was characterized by the maximal cola cantabrica (Braña et al., 1990), Phoenico- decrease of the morphological characters, lacerta kulzeri (Rizk & Nassar, 2015) and with a disappearance of the lumen in the Phoenicolacerta laevis (Hraoui-Bloquet, seminiferous tubes, and only the presence 1985; Hraoui-Bloquet & Bloquet, 1988).

6 SPERMATOGENESIS CYCLE OF THE WALL LIZARD OF DJURDJURA

7 MAMOU ET AL.

Figure 4: Testis and epididymis histological sections during the reproductive cycle of P. vaucheri. A and B: Sexual activity phase (April, May, June). A: Seminiferous tubules contained all cell cate- gories. Spermatogonia (Spg), primary spermatocytes (SP), secondary spermatocyte (SS), sperma- tid (Spt) and spermatozoa (Spz). B: Observation of spermatozoa in the epididymis lumen. Epithe- lium layer (EL); C and D: Sexual rest phase (July). C: Seminiferous tubules with only spermatogo- nia (Spg) and some primary spermatocytes (SP). D: Empty epididymis lumen; E and F: Early re- crudescence phase (August). E: Seminiferous tubules at the beginning of spermatocytogenesis. F: Empty epididymis lumen; G and H: Autumnal spermiogenesis (September and October). G: All cell categories were observed in the seminiferous tubules. H: Epididymis lumen remains empty.

This autumnal spermiogenesis has been 2009; Al-Amri et al., 2013). However, the interpreted as an abortive spermatogenesis epididymis cycle of P. vaucheri was similar (Angelini et al., 1979), or as a potential to that of Podarcis bocagei (Galán, 1996), P. second reproductive season (Carretero, muralis (Saint-Girons & Duguy, 1970), Iber- 2006). olacerta monticola (Braña et al., 1990), In addition, no follow-up was possible Acanthodactylus erythrurus (Carretero & during winter because of the local climate Llorente, 1995), Psammodromus algirus characterizing the Tala Guilef sector. (Carretero & LIorente, 1997), and seems Snowing time remained from November different from that of Timon lepidus until March in this region (Hamdine et al., (Castilla & Bauwens, 1990) and Phoenico- 1993), reducing the period of lizards’ activ- lacerta laevis (Hraoui-Bloquet, 1985; Hra- ity to seven months, and thus influencing oui-Bloquet & Bloquet, 1988), where the the reproductive cycle. Wall lizard Podarcis secondary sexual characters are well de- vaucheri from Djurdjura did not exhibit veloped in both autumn and spring. Rizk & any sperm storage in the epididymis dur- Nassar (2015) reported also this post- ing hibernation. Even though spermatozoa hibernation activity in Phoenicolacerta kul- were already present in autumn, these re- zeri, with the presence of spermatozoa and mained in the testes. Hence, males can be secretory granules in the epididymis only regarded as unfertile during this period in spring. However, the occurrence of (Angelini et al., 1979; Roig et al., 2000; spermatozoa in the testes and epididymis Carretero et al., 2006a; Rizk & Nassar, in spring and autumn was reported in Li- 2015). They became fertile in spring only olaemus species from Patagonian, Argenti- when spermatozoa migrated to the epidi- na (Medina & Ibargüengoytía, 2010). dymis. Moreover, during the phase of sex- Both the histological analysis of testes ual activity, a hypertrophy of the epididy- and field observations showed the repro- mis resulted in an increase of epithelium duction period lasting three months, from height and accumulation of secretory April to June. In the field, several male- granules in its lumen. These various sub- female pairs were seen in copulation posi- stances secreted by the epithelial cells tions, females with recent copulation scars seem to perform a significant role in the were found, and those captured in June spermatozoa maturation (Ferreira et al., were pregnant (pers. obs.). This led to

8 SPERMATOGENESIS CYCLE OF THE WALL LIZARD OF DJURDJURA think that spermatogenesis and oogenesis viewers for their comments on the earli- are synchronous, and that mating really er version of the manuscript. Also, we lead to fertilization. If so, the cycle of re- sincerely thank Mr Meribai Y. Director production of P. vaucheri would belong to of the Djurdjura national park for per- the associated type, which is common in mission. We are especially grateful to temperate climate (Hraoui-Bloquet, 1985; Moussa and Mohand for their unfailing Hraoui-Bloquet & Bloquet, 1988; Amat et support during our fieldwork. al., 2000; Roig et al., 2000; Carretero et al., handling followed humane treatment, 2006a). According to the definition of and was in agreement with current laws Whittier & Crews (1987), in the associated of Algeria. We are also sincerely grateful reproductive pattern, male mating behav- to Dr. Merzouk Mamou for his help and ior coincides with the time of the year at to enable us to carry out the first steps of which gonads are enlarged and actively this work in Laboratory of analytical producing gametes, while in the dissociat- chemistry, Tizi Ouzou University. ed reproductive pattern, spermatogenesis References occurred before mating and consequently the gametes are stored until the mating Abu-Zinadah, O.A. (2008). Variation in tes- period (e.g. in epididymis or spermato- ticular histology of the spiny tailed lizard phores). Uromastyx aegyptius microlepis during hibernation and active periods. Pakistan In conclusion, data presented here al- Journal of Biological Sciences 11: 1615–1619. lowed us to shed light on some of the Al-Amri, I.S.; Mahmoud, I.Y.; Waring, C.P.; adaptive strategies used by the wall lizard Alkindi, A.Y.; Khan, T. & Bakheit, C. Podarcis vaucheri in Djurdjura Mountain. (2012). Seasonal changes in plasma ster- Our results showed that timing of sper- oid levels in relation to ovarian steroido- matogenesis reflect the "Mediterraneity" of genic ultrastructural features and proges- the reproductive strategy of this species terone receptors in the house gecko, Hem- with an adaptive response to altitudinal idactylus flaviviridis, in Oman. General and conditions. An early interruption of the Comparative Endocrinology 177: 46–54. spermatic activity, a short sexual rest and Al-Amri, I.S.; Mahmoud, I.Y.; Waring, C.P.; Alkindi, A.Y.; Khan, T.; Bakheit, C. & Al an early resumption of spermatogenic ac- -Mawali, K.M. (2013). The reproductive tivity represent adaptations allowing com- cycle of the male house gecko, Hemidacty- pensating both the long hibernation period lus flaviviridis, in relation to plasma ster- and the late emergence in spring (Saint- oid concentrations, progesterone recep- Girons & Duguy, 1970). However, compar- tors, and steroidogenic ultrastructural ative studies between the different evolu- features, in Oman. General and Compara- tionary lineages will be necessary to assess tive Endocrinology 187: 23–31. the geographical variations in their repro- Aldridge, R.D. (1975). Environmental con- trol of spermatogenesis in the rattle ductive characteristics. snake Crotalus viridis. Copeia 1975: 493- Acknowledgements 496. Amat, F.; Llorente, G.A. & Carretero, M.A. We are grateful to the anonymous re- (2000). Reproductive cycle of the sand

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