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Herpetology Notes, volume 10: 537-545 (2017) (published online on 16 October 2017)

Sperm retention in flavipunctatus Rüppell, 1835 (: ), with a brief review of sperm storage in

Herbert Rösler1, Wolfgang Wranik2 and Hinrich Kaiser3,*

Abstract. We here describe sperm retention in Pristurus flavipunctatus Rüppell, 1835 for the first time. During three different time intervals, a female kept isolated from males for a period of 250–286 days produced nine, 19, and 24 fertile egg clutches, which must have been fertilised using stored sperm. Pristurus flavipunctatus is revealed as the third among the Sphaerodactylidae, for which sperm storage has been confirmed. We also provide a brief review of sperm storage in geckos.

Zusammenfassung. Erstmalig wird von Pristurus flavipunctatus Rüppell, 1835 eine Spermaspeicherung beschrieben. Ein vom Männchen für 250–286 Tage getrennt gehaltenes Weibchen produzierte in drei unterschiedlichen Zeiträumen neun, 19 und 24 Gelege, die durch gespeichertes Sperma befruchtet wurden. Damit ist Pristurus flavipunctatus die dritte Art der Sphaerodactylidae für die eine Spermaspeicherung nachgewiesen ist. Wir präsentieren außerdem einen kurzen Überblick über Spermaspeicherung in Geckos insgesamt.

Keywords. Squamata, Sauria, , Sphaerodactylidae, Pristurus flavipunctatus, sperm storage.

Introduction , Hildebrand (1929) appears to be the first to have confirmed sperm storage ability experimentally Sperm storage is the capacity of an to receive in the turtle Malaclemys terrapin centrata, before a quantity of sperm during a particular mating episode, Kopstein (1938) reported the details of sperm storage and then retain the sperm for a period of time in order in Xenochrophis vittatus (as Natrix vittata), Rhabdophis to produce one or several fertilised egg clutches or subminiatus (as N. subminiata), R. chrysargos (as juveniles in subsequent time periods. This phenomenon N. chrysarga), Ptyas mucosus, P. korros, and Boiga is known across a diverse number of animal groups, multomaculata (as B. multimaculata). Felix Kopstein including both (e.g., Birkhead and Møller, (1893–1939) was also the person who coined the term 1993; Holt, 2011) and (e.g., Uhl, 1996; amphigonia retardata to describe the process (Petzold, Peretz-Staples et al., 2007; Dillen et al., 2009). Among 1984; Adler, 1989). At this point, sperm storage in reptiles has been documented widely in a variety of crocodile, turtle, , and species, either via observations during captive breeding or by morphological examination of 1 Sektion Herpetologie, Senckenberg Naturhistorische the female reproductive tract (e.g., Bellairs, 1969; Obst Sammlungen Dresden, Museum für Tierkunde, et al., 1984; Petzold, 1984; Kluge and Schuett, 1986; Königsbrücker Landstraße 159, 01109 Dresden, Germany Heatwole and Taylor, 1987; Olsson and Madersen, 2 Institut für Biowissenschaften, Universität Rostock, Albert- 1998; Sever and Hamlett, 2001; Engelmann, 2006; Einstein-Straße 3, 18051 Rostock, Germany Eckstut et al., 2009a). In this regard, it is noteworthy 3 Department of Biology, Victor Valley College, 18422 Bear that the more recent evidence is based primarily on Valley Road, Victorville, California 92395, USA; and morphological examinations, which merely confirmed Department of , National Museum of Natural History, Smithsonian Institution, Washington, DC the ability to store sperm, but which did not investigate 20013, USA what the viability of stored sperm and the ability to * Corresponding author E-mail: [email protected] produce clutches from it might be. 538 Herbert Rösler et al.

2005). The first proof for sperm storage in the diurnal Middle-Eastern sphaerodactylid Pristurus Rüppell, 1835 was provided by Rösler (2016), based on observations in P. carteri. We here present the second instance of sperm storage in the genus Pristurus, based on a three-year observation period of P. flavipunctatus Rüppel, 1835.

Material and Methods Characteristics of Pristurus flavipunctatus.— Species of Pristurus can be divided into two groups based on their overall body shape and relative tail length. One of these, represented by P. carteri, has a relatively stocky body build and a short tail (snout–vent length [SVL] > tail length [TL]). The other, exemplified by P. flavipunctatus (Fig. 1) has a narrow body and a long tail (SVL < TL). At an SVL of 35–40 mm, P. flavipunctatus belongs to the smaller Pristurus species (Rüppell, 1835; Figure 1. Adult female Pristurus flavipunctatus from Al Scortecci, 1928; Loveridge, 1947; Henkel and Schmidt, Hudaydah (northern ). Approximate snout–vent length 2003). All individuals of P. flavipunctatus observed in 38 mm. Photo by Herbert Rösler. the northern part of Yemen (H. Rösler, pers. obs.) were coloured greyish brown with inconspicuous dorsal and lateral patterns (Fig. 1). Other populations of P. flavipunctatus may have more contrasting patterning As a group, geckos have a variety of specialized (Baha el Din, 2006; Sindaco and Jeremčenko, 2008; reproductive characteristics, including eggshell Largen and Spawls, 2010). morphology, clutch size, and egg deposition behaviour. Provenance and .—During fieldwork in the Sperm storage is one of these characteristics (see Rösler, spring of 2009, two adult individuals of P. flavipunctatus

Figure 2. City habitat of Pristurus flavipunctatus in Al Hudaydah (northern Yemen). The red arrow marks the specific place of capture. Photo by Wolfgang Wranik�. Sperm retention in Pristurus flavipunctatus 539

Figure 3. Natural habitat of Pristurus flavipunctatus in Al Arj (northern Yemen). Photo by Wolfgang Wranik.

were collected in two very different . A female for 14 h to achieve a temperature of 29–32°C (timed was found basking on the wall surrounding a residence to increase to 35–37°C under the spotlight) during the within the city limits of Al Hudaydah (Fig. 2), and a day, with a nightly temperature reduction of 5–7°C. In male was found active in a mangrove tree (Avicennia the “winter,” the number of light hours was reduced to marina) in Al Arj (Fig. 3), a coastal locality several 10 h, with temperatures of 27–29°C (up to 33°C under kilometres distant from the outskirts of Al Hudaydah. the spotlight) during the day, and cooler by 7–11°C at These geckos were transported to Germany in separate night. During both simulated seasons, geckos had cooler small containers and were subsequently established in a refugia available, where the temperature was 4–6°C single terrarium. lower than elsewhere in the terrarium. Twice a week, Terrarium setup.—To accommodate the pair, a water was sprayed into the terrarium to create a relative terrarium of length/width/height dimensions 28 x 23 humidity averaging 65%. For the subsequent separation x 35 cm with a clay-sand mixture substrate of 3–4 cm of the female, a second identically constructed and depth was used. The microhabitat was shaped using flat, similarly equipped terrarium was built, and the same vertically applied bark pieces and finely branched boughs seasonal simulations were employed (with the same to provide diverse hiding places and climbing structures. temperature and relative humidity values). The captive The terrarium was illuminated using fluorescent bulbs individuals were fed crickets (Gryllus assimilis) and (non-daylight, non-heating), supplemented by timed (Alphitobius diaperinus, Tenebrio molitor). spotlights (to produce warm areas and to supply a Variety was produced by periodically introducing small amount of ultraviolet radiation). The climate wingless fruit ( hydei), small wolf inside the terrarium was set to simulate summer and (Lycosidae), jumping spiders (Salticidae), and winter seasons. During the “summer,” lights were on weevils (Acanthoscelides obtectus). 540 Herbert Rösler et al.

Table 1. Specifics of contact times and egg-laying periods, as well as information about clutches and sperm storage of Pristurus flavipunctatus. Table 1. Specifics of contact times and egg-laying periods, as well as information about clutches and sperm storage of Pristurus flavipunctatus.

Fertilization Minimal Sperm Storage Female + Male Female Only Egg-Deposition Periods (A–C) No. of Clutches success (%) (days)

1 Apr 2009–17 Oct 2012 18 Oct 2012–1 Jul 2014 April 2013–30 Jul 2013 (A) 9 100 272

2 Jul 2014–12 Jul 2014 13 Jul 2014–17 Oct 2015 16 Jul 2014–7 May 2015 (B) 19 94 286

18 Oct 2015–4 Nov 2015 5 Nov 2015–31 Dec 2016 8 Nov 2015–28 Jul 2016 (C) 24 96 250

Results (number of produced clutches per month) was lower during the time the female was housed with the male Acclimation.—From their arrival in March 2009 until than when housed by herself (1.86 vs. 2.17 eggs per October 2012, the male and female P. flavipunctatus month, respectively). were kept in the same terrarium. During this time span, the female produced 78 clutches (91% fertilized) that Discussion each consisted of a single egg, during all months of the year. The production of multiple egg clutches or neonates Cohabitation.—The pair was separated for the first following one-time insemination brings a variety of time in October 2012, and the female was introduced advantages to the amniotes capable of doing so. For into the male’s terrarium only for short periods in order example, Petzold (1984) showed that sperm storage to observe mating behaviour. The female individual allowed organisms to increase the reproductive rate was moved to a separate enclosure because even of a population independent of fluctuations in density though individuals of both sexes in the genus Pristurus (affecting the ability of resources) or gender parity are territorial, males defend their territories more aggressively. During Summer 2014 they were kept together for 11 days and in Winter 2015 for 18 days. In both instances, mating behaviour (male courtship) was observed immediately after the individuals were placed together, but there was no actual mating attempt. Once gravidity could be observed (by lateral swelling on one side of the lower abdomen), the pair was separated again. Sperm storage.—The oviposition periods, during which the female laid eggs while isolated from the male (Table 1), are listed as Periods A (2013), B (2014–15), and C (2016–17). During the entire time span of these observations (2013–2017), the female produced 52 egg clutches, of which 97% were fertilized. The first two clutches during Period A were deposited during April 2013 (Table 1; Fig. 4), ca. 5 mo after the removal of the male (achieving an “overwintering” of sperm). During Periods B and C the female produced clutches continuously during the time immediately following the “visit” by the male (Table 1; Fig. 4). Gestation in P. flavipunctatus was 7–27 d (13.9 ± 4.4 d, n = 52). Omitting a mean number of days to account for gestation, these Figure 4. Schematic of time periods for male-female contact data show that the female P. flavipunctatus was able to and reproductive episodes for Pristurus flavipunctatus during store fertile sperm for 250–286 d. Clutch production 2012–2016. Sperm retention in Pristurus flavipunctatus 541

(affecting the availability of males). In species with retained sperm or via egg retention of already fertilized shifting gonadal activity (e.g., when acyclical or eggs (see López-Jurdao et al., 1982; Rhode, 1991), shortened in males), stored sperm enables females to since it is not possible to determine unequivocally in produce eggs independent of the reproductive readiness vivo when specifically ovarian follicles are fertilized. of males (Heatwole and Taylor, 1987). Sperm storage Similarly, without a thorough in situ examination it is not is also instrumental in the expansion of a species’ possible to determine if, or how many, fertilized eggs are range, such as when females with stored sperm raft retained in the ovaries. It is known for geckos with fixed across marine barriers and colonize islands. Similar to clutch sizes that their ovaries are capable of supporting parthenogenetic species, a single female with stored several follicles at different developmental stages, as sperm would be able to produce enough offspring to observed in Tenuidactylus caspius (3–8 follicles; Hojati become the founder of a new population (Yamamoto and et al., 2013). In species that produce only a single egg Ota, 2006). Furthermore, while on the one hand sperm per clutch, only one egg reaches full maturity at any storage can reduce the need to reproduce in a stressful point in time, alternating between the left and right environment, such as at high population densities, on oviducts. Arnold (1993) reported the presence of two the other hand it allows for a sufficient reproductive rate eggs in the oviducts of pregnant females of several when males are scarce, such as when the population species of Pristurus, but without information regarding density is low (as in areas with less than optimal habitat the degree of follicle maturity. Clutches (number of conditions along edges and in ecological transition clutches observed in parentheses) of P. carteri (91), P. zones). In complex habitat types, where the frequency insignoides (1), P. flavipunctatus (130), P. obsti (153), of encountering a suitable mate is strictly limited P. samhaensis (1), P. sokotranus (64), and Pristurus (e.g., in ), sperm storage contributes to the sp. (29) invariably comprised only a single egg, but the stabilization of the population structure because even short interval between clutch production (a minimum limited encounters can result in multiple reproductive interval of only 4 d was observed) allows the conclusion episodes. Even adverse climate conditions can be that two eggs develop essentially simultaneously (H. bridged by sperm storage (e.g., through the production Rösler, unpubl.). of fertile eggs following periods of cold, drought, Long time periods between egg deposition, such or rains that would ordinarily not allow normal egg as those observed to last up to several years in turtles development). and (Petzold, 1984) are generally taken as an Clutches of many squamates that reproduce mono-, indication of long-term sperm storage. In contrast bi- or multicyclically (i.e., that use sperm retained from to the time spans observed there, it is possible that a single mating for the production of one, two, or several sperm storage is strictly short-term, covering a single egg clutches, respectively) generally comprise several reproductive period (monocyclic reproduction). An eggs (see Fitch, 1982), but several groups of example for the occurrence of typical short-term sperm evolved alternative reproductive strategies. These storage is Hemidactylus turcicus, where sperm can include a prolonged frequency with which eggs can be remain in the oviducts from May–August (Eckstut et produced, in combination with a smaller clutch size. al., 2009b). Such multi-clutch strategies, with clutch sizes reduced The reproductive cycle (spermatogenesis, to one or two eggs, have been shown to exist among vitellogenesis) in P. flavipunctatus in nature is still other taxa in the geckos and dibamids (Underwood, unknown. Egg-bearing females, eggs, or hatchlings of 1954; Kluge, 1967; Greer, 1985). Stored sperm allows P. flavipunctatus and Pristurus sp. (sensu Badiane et al., uninterrupted ovulation and egg formation in females 2014) were observed in Yemen during the months of and therefore avoids the higher physiological cost of November–January and March (H. Rösler, pers. obs.). ramping up hormonally to the production of multiple This may indicate that the reproductive period of P. eggs and clutches on a larger scale. flavipunctatus is relatively extensive, which is typical Included in the evolutionary functionality of sperm of tropical geckos (Rösler, 2003). The need to be ready storage is also the possibility of sperm competition, to lay eggs over an extended reproductive period is, whereby after mating with two or more males the sperm perhaps, also the reason why long-term sperm storage of one of the suitors is favoured (Birkhead, 1995, 1998; Bussière et al., 2006; Olsson et al., 2007). However, it is  The designation Pristurus sp. follows Badiane et al. (2014) difficult to determine whether delayed clutch production and identifies an undescribed species of Pristurus with simi- is ultimately due to de novo fertilization of egg cells via larities to P. rupestris from southern Yemen. 542 Herbert Rösler et al. in this species is an advantage to females, as indicated Eublepharis macularius, Haemodracon riebeckii, by the shown ability to retain fertile sperm over a 9-mo Hemidactylus frenatus, Nephrurus asper, period in captivity. dubia, P. guentheri, , Pristurus ���sp., � It is difficult to determine which internal or external Pseudogekko smaragdinus. These species are capable factors steer short-term vs. long-term sperm storage. It of storing sperm from 93–430 d (see Appendix�).� appears unlikely that external factors (e.g., temperature, humidity, nutrition) would have produce or the 5- Acknowledgments. We thank Hidetoshi Ota and Salvador mo break in egg-laying activity by the inseminated P. Carranza for providing us with their publications. Our special flavipunctatus-female during Period A (mid-October thanks go to Adel Alhababy of Hudayah University for his 2012 through late March 2013), since there was no expertise in facilitating fieldwork in Yemen. �������� ��� collection were carried out under permits issued to Hudayah variance in these values. University by the Ministry of Water and the Environment, and According to Hedges and Vidal (2009), geckos are specimens were exported in accordance with Section 2, Article divided into two main lineages, the Pygopodomorpha and 52 of the Yemeni Customs Law. the Gekkomorpha. Reports of sperm storage are available for species of , , References , , , and Sphaerodactylidae. There are so far no reports for Adler, K. (1989): Contributions to the history of herpetology. Society for the Study of Amphibians and Reptiles, Contributions sperm storage in (see Appendix). Whereas to Herpetology 5: 1–202. the ability to store sperm is well known in geckos in Arnold, E.N. (1993): Historical changes in the ecology and principle, it has only been confirmed via either in situ behaviour of semaphore geckos (Pristurus, Gekkonidae) and observations or experimentally in about 1.7% of known their relatives. Journal of Zoology 229 (3): 353–384. species. It is perhaps easiest to verify sperm storage via Badiane, A., Garcia-Porta, J., Červenka, J., Kratochvil, L., Sindaco, morphological examination, the sole method by which R., Robinson, M.D., Morales, H., Mazuch, T., Price, T., Amat, F., sperm storage was identified in Coleonyx variegatus, Shobrak, M.Y., Wilms, T., Simó-Riudalbas, M., Ahmadzadeh, F., Papenfuss, T.J., Cluchier, A., Viglione, J., Carranza, S. 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Appendix. Literature records of sperm storage in species of geckos in the families ���������������������������������� Appendix Eublepharidae, Gekkonidae, Phyllodactylidae, and Sphaerodactylidae. Literature records of sperm storage in species of geckos in the families Carphodactylidae, Diplodactylidae, Eublepharidae, Gekkonidae, Phyllodactylidae, and Sphaerodactylidae.

Family Species Reference Evidence/Time Period Carphodactylidae Nephrurus asper Couper (1996) > 277 d Phyllurus platurus Green (1973) through the Winter Phyllurus platurus Mo (2014) through the Winter Saltuarius wyberba Girling et al. (1998) sperm in the cloacal area How et al. (1990) no time provided Diplodactylidae and species Todd (2003) sperm in the oviduct Girling et al. (1997) through the Winter Woodworthia maculata Girling et al. (1998) sperm in the cloacal area Woodworthia ‘Central Otago’ Cree and Hare (2016) sperm posterior in the uterine tube, 6 mo Woodworthia ‘Otago large’ Cree and Hare (2016) sperm posterior in the uterine tube, 6 mo Eublepharidae Aeluroscalabotes felinus Rösler (2007) 293 d Aeluroscalabotes felinus Wolf (2009) 430 d Coleonyx variegatus Cuellar (1966) sperm in the infundibulum Coleonyx variegatus Sánchez-Martinez et al. (2007) sperm in the cloacal/uterine area (cervix uteri) Eublepharis macularius Minton (1966) 4 mo Eublepharis macularius Goin and Goin (1971) 4 mo Eublepharis macularius Parker (1972) no time provided Gekkonidae Christinus marmoratus King (1977) through the Winter in the cloacal area Hemidactylus frenatus Fläschendräger (1985) > 160 d Hemidactylus frenatus Murphy-Walker and Haley (1996) 252 d Hemidactylus frenatus Yamamoto and Ota (2006) 382 d Hemidactylus mabouia Nogueira (2008) sperm in the infundibulum/uterus (uterine tubus) Hemidactylus mabouia Nogueira et al. (2011) sperm in the infundibulum/uterus (uterine tubus) Hemidactylus turcicus Girling et al. (1998) sperm the cloacal area Hemidactylus turcicus Eckstut et al. (2009a) sperm in the infundibulum Hemidactylus turcicus Eckstut et al. (2009b) sperm in the infundibulum/uterus (uterine tubus), 5 mo Hemidactylus platyurus Church (1962) no time provided Heteronotia binoei Whittier et al. (1994) sperm in the infundibulum and cloacal area Lepidodactylus ‘lugubris’ Saint Girons and Ineich (1992) sperm in the uterus Nactus multicarinatus Eckstut et al. (2009a) sperm in the infundibulum Nactus multicarinatus Eckstut et al. (2009c) sperm in the infundibulum (February, April) Nactus pelagicus Eckstut et al. (2009c) follicles and sperm in the oviduct, but not simultaneously Phelsuma dubia Osadnik (1984) no time provided Phelsuma dubia Osadnik (1987) sperm in the upper uterus, 145 d Phelsuma guentheri Bloxam and Vokins (1978) 143–232 d Pseudogekko smaragdinus Rösler (2005) > 5 mo Phyllodactylidae Haemodracon riebeckii Rösler (2005) 93 d Phyllodactylus homolepidurus Cuellar (1966) sperm in the infundibulum Thecadactylus rapicauda Sánchez-Martinez et al. (2007) sperm in the cloacal/uterine area (cervix uteri) Sphaerodactylidae Gonatodes albogularis Sánchez-Martinez et al. (2007) sperm in the cloacal/uterine area (cervix uteri) Pristurus carteri Rösler (2016) 265 d Pristurus flavipunctatus this study 286 d Pristurus sp. Rösler et al. (2017) 320 d

Accepted by Daniel Portik