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Male Reproductive Behaviour of Naja Oxiana (Eichwald, 1831) in Captivity, with a Case of Unilateral Hemipenile Prolapse

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Male Reproductive Behaviour of Naja Oxiana (Eichwald, 1831) in Captivity, with a Case of Unilateral Hemipenile Prolapse Herpetology Notes, volume 11: 1061-1064 (2018) (published online on 19 December 2018) Male reproductive behaviour of Naja oxiana (Eichwald, 1831) in captivity, with a case of unilateral hemipenile prolapse Alireza Nasoori1,2, Ali Taghipour3, and Bruce A. Young4,* Abstract. The Central Asian cobra, Naja oxiana, is a species with an uncertain conservation status that is rarely bred in captivity. Male N. oxiana exhibit a dissociated breeding pattern, in which mating behaviour coincides with reduced levels of testosterone; the cues that promote copulatory behaviour in this species are not fully understood. Herein we report a case where prolonged copulation led to hemipenile prolapse in a specimen of N. oxiana. When the initial therapeutic intervention failed to relieve the condition the affected hemipenis was amputated, after which the snake successfully recovered. In order to minimize exaggerated copulatory behaviour we recommend keeping this species in segregated enclosures. A better understanding of the cues that trigger normal and exaggerated copulatory behaviour in this species would facilitate its captive propagation. Keywords. Naja oxiana, hemipenile prolapse, copulatory behaviour Introductionntroduction snakes, including garter snakes (genus Thamnophis), exhibit a dissociated reproductive pattern with low The male copulatory organ in snakes is the hemipenis; androgen levels during the mating period (Tam et al., the separate right and left hemipenis is connected to the 1969; Tumkiratiwong et al., 2012; Schořálková et al., testis of the same side. At rest the hemipenes are pulled 2017). In N. oxiana, and most other snake species with into the tail by a retractor muscle; during copulation only dissociated reproduction, the triggers for copulatory one hemipenis is erected and inserted into the female’s behaviour are not well known. cloaca (Kelly, 2002; Funk, 2005; Mitchell and Tully, Cloacal prolapse (CP) is a common reproductive 2015).. Hemipenal erection is the result of engorgement disorder in reptiles (Rivera, 2008; Alworth et al., 2011), with blood (Kelly, 2002; Rosenthal et al., 2008). typically caused by gastrointestinal disease, metabolic Increased androgen levels are considered the main bone disease, or reproductive disorders (Hedley and trigger for mating behaviours in male snakes (Taylor and Eatwell, 2014). Hemipenile and penile prolapses DeNardo, 2011). However, Naja oxiana, as well as other (HP and PP) are the most common forms of CP in reptiles (Hedley and Eatwell, 2014). Some (abnormal) reproductive behaviours (such as excessive and chronic mating) are associated with an increased incidence of HP (Hedley and Eatwell, 2014; Podhade and Harne,, 1 Graduate School of Veterinary Medicine, Hokkaido 2014). Two main therapeutic approaches have been University, Sapporo 060-0818, Japan. advanced for Wreatinging HP, namely (1) fixation of the 2 Pasteur Institute of Iran, Production and Research Complex, hemipenis by suture, or (2) surgical amputation of the Biotechnology Processes Developing Center, Karaj hemipenis (%arten, 2005; Rivera, 2008; Alworth et al., 3159915111, Iran. 2011). Herein we describe HP management by surgical 3 Department of Clinical Sciences, School of Veterinary Medicine, Islamic Azad University, Karaj Branch, Karaj amputation. Furthermore, we elaborate on possible 31485-313, Iran. underlying behavioural and physiological factors that 4 Department of Anatomy, Kirksville College of Osteopathic likely led to the abnormal or exaggerated mating in this Medicine, A.T. Still University, Kirksville, MO, 63501, case. USA. * Corresponding author. E-mail: [email protected] 1062 Alireza Nasoori et al. Clinical Findings episodes on 20 July 2016, we observed that one of the males engaged in prolonged copulation and thereafter Hemipenal prolapse.—Naja oxiana (Fig. 1) is a presented with unilateral hemipenile prolapse (Fig. 2). terrestrial elapid occurring in the Transcaspian region We isolated the snake, which was lethargic and from northeast Iran to northern India (Nasoori et anorectic. For the first four days after isolation, we al., 2016). The individual described in this case was used a non-surgical therapeutic approach to promote captured in Sabzevar, Khorasan Province, northeastern the deflation and retraction of the prolapsed hemipenis. Iran (ca. 36°13’N, 57°40’E; Nasoori et al., 2014).. This area has a desert climate with a yearly average The prolapsed organ was rinsed daily with normal temperature of 15.6°C. The warmest month is July saline and treated with ointments containing lidocaine, (average temperature 30°C), the coldest month is hydrocortisone, and soluble lubricant (Frye, 1991). At January (average temperature 0.6°C). the end of the therapy period there was no observable Naja oxiana is a solitary, oviparous species, whose change in the size of the protruded hemipenis, and the sexual cycle is poorly known. The captive colony at animal did not appear to improve. In order to prevent the Pasteur Institute of Iran in Karaj, Iran (35°50’N, the possibility of subsequent necrosis and infection wee 50°59’E; colony temperature ca. 26°C), houses 16 decided to amputate the prolapsed hemipenis. individuals (four males, 12 females) that exhibit mating Anaesthesia and surgery.—Thirty minutes prior to the behaviour and oviposit in July. During one of the mating procedure, the snake’s head and forebody were pinned against the substrate using a handling tool fitted with an expanded pad at the end. A short segment of the cobra’s mid-body was isolated by hand, so that injections could be safely administered to the axial muscles. The animal received a 2.5 mg/kg intramuscular injection of gentamicin (Gentamicin 5%, DarouPakhsh, Iran) as prophylaxis, followed by intramuscular injection of 2 mg/kg diazepam (Zepadic, 10 mg/2ml, CaspianTamin, Iran) for immobilization. Lidocaine hydrochloride (0.2 ml, Lignodic 2%, CaspianTamin, Iran) was injected into the root, body, and head of the prolapsed hemipenis to induce local anaesthesia. The prolapsed hemipenis and the surrounding area were disinfected with povidone iodine (10%, Iran), followed by a normal saline rinse. The prolapsed hemipenis was ligated with a non- absorbable silk 2-0 suture (Supa, Iran) at a distance of 2 mm distal to the root, and amputation was performed just distal to the ligation. The animal was checked for bleeding repeatedly immediately after the procedure and, when none was observed it was returned to its (sterile) isolation cage. Recovery.—Daily, the snake was gently pinned (as described above) and the amputated area was rinsed with povidone iodine and normal saline, followed by the application of oxytetracycline spray (OTC, Vetaque, Iran) to the surgical area. On Day 2 of recovery, 10 mg/kg Enrofloxacin (Hipralona Enro-I, 10%, Hipra, Spain) and Vitamin B complex (Osve, Iran) were intramuscularly administered. On Day 3 after the Figure 1. Naja oxiana in life, showing an ovipositing female procedure, the snake raised its head and neck, expanded (main image) and a close up of the head and neck (insert). its hood, and appeared fully alert to peripheral cues. On Photos by Alireza Nasoori. this day the ligature was removed from the base of the Male reproductive behaviour of Naja oxiana in captivity 1063 Figure 2. Male Naja oxiana showing a prolapsed hemipenis in two views. Photos by Alireza Nasoori. amputated hemipenis without bleeding or complication, or were fertilized by sperm the females were storing in and the snake was judged to have fully recovered. their bodies. Sperm storage for periods of several months have been well documented in snakes (Halpert et al., Discussioniscussion 1982) and there are claims of viable sperm being stored for over five years (e.g., Magnusson, 1979). Male cobras Treating prolapses.—Amputation of prolapsed typically have postnuptial (or Type II of Lance, 1998) hemipenis is generally recommended, in part, because reproduction cycles (Taylor and DeNardo, 2011), which it prevents necrosis and subsequent infection (Frye, means they initiate spermatogenesis months before 1991). Since in snakes the hemipenes are paired, and mating, and store spermatoza in their vas deference (or do not function in excretion, unilateral amputation of a epididymis) before copulation (Lofts et al., 1966; Tam prolapsed hemipenis compromises neither urination nor et al., 1969; Tumkiratiwong et al., 2012). In vertebrates, future copulation (Kelly, 2002; Funk, 2005; Mitchell and including reptiles, androgens are considered a key Tully, 2015). In the present case, the individual recovered trigger for male courtship and copulatory behaviours rapidly after the hemipenectomy, which is consistent (Schořálková et al., 2017). In some species, including with earlier reports of HP and PP management (Nisbet cobras, the level of testosterone is not high at the time et al., 2011; Da Silva et al., 2013; Podhade and Harne, of mating (dissociated reproduction; Tam et al., 1969; 2014). Nevertheless, treatment and management of CPs Tumkiratiwong et al., 2012; Schořálková et al., 2017). In (including PP and HP) are not always promising. About these forms it remains unclear what cues are triggering 27% of prolapse cases recur after the prolapsed organ mating behaviour. is physically replaced (with or without an overlying Prolonged copulation is an evolutionary strategy to suture), and a nearly equal percentage of cases end in the increase mating success in male snakes through sperm death (or euthanasia) of the animal (+edley and Eatwell, competition (Shine, 2003). However,
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