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The social behaviour of teiid lizards, including courtship and mating, is difficult to study in free-ranging individuals due largely to their wide foraging, large home ranges, and general wariness (e.g. Vitt and Price, 1982; Censky, 1995; Lopes and Abe, 1999; Ribeiro et al., 2011). The reproductive behaviour of the common tegu, Salvator merianae (Duméril & Bibron, 1839), based on captive individuals maintained in enclosures that resembled their natural habitat, is thoroughly described and illustrated in Lopes and Abe (1999). Courtship and attempted mating with dead females (necrophilia) is a behaviour recorded for various lizard species (e.g. How and Bull, 1998; Fallahpour, 2005; Brinker and Bucklin, 2006; Costa et al., 2010). A detailed account on necrophiliac behaviour of a teiid lizard, the green ameiva Ameiva ameiva (Linnaeus, 1758), was recently reported by Costa et al. (2010). Herein I describe necrophilia for another teiid, the large common tegu Salvator merianae. Males were recorded to courtship and attempting to mate with a dead conspecific female for two consecutive days at an urban park in South-eastern Brazil. The necrophiliac behaviour displayed by male tegus was recorded at the Parque Ecológico Prof. Hermógenes de Freitas Leitão Filho (22°48’42”S, 47°04’21”W, 584 m a.s.l.), Campinas, São Paulo, South-eastern Brazil. This park has a total area of about 13 ha, with a large pond surrounded by trees, bushes and grass patches, and harbours a sizeable population of the common tegu (Sazima and D’Angelo, 2013). I observed the tegus in two afternoons in September 2013, with bare eye and through a 70-300 mm telephoto zoom lens mounted on a camera from a distance of 2-5 m. Throughout the observational sessions I used ad libitum sampling, which is adequate to record rare events (Altmann, 1974). Voucher digital photographs of the tegu necrophiliac behaviour are housed on file at the Museu de Zoologia da Universidade Estadual de Campinas (ZUEC). On 20 September, I recorded a large male (about 40 cm snout-vent length, SVL) that approached a freshly dead female (34.7 cm SVL) and tongue-flicked her body at 1707h. The male attempted to court, and mate with, the female from 1708 to 1713h (5 min) when a group of geese approached and caused him to flee. Air temperature was 29.6º and air humidity was 47%. The following afternoon (21 September), I recorded a smaller male (about 35 cm SVL) already engaged in courtship and mating attempts. The female’s position was opposite to that of the previous afternoon, and she had a bloated body and emitted a strong rotting smell. Blow flies (Calliphoridae) and flesh flies (Sarcophagidae) were on her snout and nearby twigs. This male attempted to court, and mate with, the female from 1551 to 1640h (49 min) when he tongue-flicked the head the female and left. Air temperature was 32.3º C and air humidity was 36%. The males behaved similarly in the presence of the dead female in the first and second day (Fig. 1). They tongue-flicked the head and body of the female; embraced and scratched her body with forelimbs (Fig. 1 a-f); rubbed the throat on her body, mostly on neck (Fig. 1a, c, e); opened wide the mandibles and grasped her neck and head (Fig. 1b, d); grabbed the skin at her neck with anterior teeth (Fig. 1a, c); mounted and attempted to copulate positioning their hindbody alternately at her right or left side (Fig. 1a-e); and made hindlimb movements, scratching her body during the copulatory Herpetology Notes, volume 8: 15-18 (2015) (published online on 26 January 2015) Corpse bride irresistible: a dead female tegu lizard (Salvator merianae) courted by males for two days at an urban park in South-eastern Brazil Ivan Sazima Museu de Zoologia, Universidade Estadual de Campinas, 13083-970 Campinas, São Paulo, Brazil. E-mail address: [email protected]

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Page 1: Corpse bride irresistible: a dead female tegu lizard

The social behaviour of teiid lizards, including courtship and mating, is difficult to study in free-ranging individuals due largely to their wide foraging, large home ranges, and general wariness (e.g. Vitt and Price, 1982; Censky, 1995; Lopes and Abe, 1999; Ribeiro et al., 2011). The reproductive behaviour of the common tegu, Salvator merianae (Duméril & Bibron, 1839), based on captive individuals maintained in enclosures that resembled their natural habitat, is thoroughly described and illustrated in Lopes and Abe (1999).

Courtship and attempted mating with dead females (necrophilia) is a behaviour recorded for various lizard species (e.g. How and Bull, 1998; Fallahpour, 2005; Brinker and Bucklin, 2006; Costa et al., 2010). A detailed account on necrophiliac behaviour of a teiid lizard, the green ameiva Ameiva ameiva (Linnaeus, 1758), was recently reported by Costa et al. (2010). Herein I describe necrophilia for another teiid, the large common tegu Salvator merianae. Males were recorded to courtship and attempting to mate with a dead conspecific female for two consecutive days at an urban park in South-eastern Brazil.

The necrophiliac behaviour displayed by male tegus was recorded at the Parque Ecológico Prof. Hermógenes de Freitas Leitão Filho (22°48’42”S, 47°04’21”W, 584 m a.s.l.), Campinas, São Paulo, South-eastern Brazil. This park has a total area of about 13 ha, with a large pond surrounded by trees, bushes and grass patches, and harbours a sizeable population of the common tegu (Sazima and D’Angelo, 2013). I observed the tegus in

two afternoons in September 2013, with bare eye and through a 70-300 mm telephoto zoom lens mounted on a camera from a distance of 2-5 m. Throughout the observational sessions I used ad libitum sampling, which is adequate to record rare events (Altmann, 1974). Voucher digital photographs of the tegu necrophiliac behaviour are housed on file at the Museu de Zoologia da Universidade Estadual de Campinas (ZUEC).

On 20 September, I recorded a large male (about 40 cm snout-vent length, SVL) that approached a freshly dead female (34.7 cm SVL) and tongue-flicked her body at 1707h. The male attempted to court, and mate with, the female from 1708 to 1713h (5 min) when a group of geese approached and caused him to flee. Air temperature was 29.6º and air humidity was 47%. The following afternoon (21 September), I recorded a smaller male (about 35 cm SVL) already engaged in courtship and mating attempts. The female’s position was opposite to that of the previous afternoon, and she had a bloated body and emitted a strong rotting smell. Blow flies (Calliphoridae) and flesh flies (Sarcophagidae) were on her snout and nearby twigs. This male attempted to court, and mate with, the female from 1551 to 1640h (49 min) when he tongue-flicked the head the female and left. Air temperature was 32.3º C and air humidity was 36%.

The males behaved similarly in the presence of the dead female in the first and second day (Fig. 1). They tongue-flicked the head and body of the female; embraced and scratched her body with forelimbs (Fig. 1 a-f); rubbed the throat on her body, mostly on neck (Fig. 1a, c, e); opened wide the mandibles and grasped her neck and head (Fig. 1b, d); grabbed the skin at her neck with anterior teeth (Fig. 1a, c); mounted and attempted to copulate positioning their hindbody alternately at her right or left side (Fig. 1a-e); and made hindlimb movements, scratching her body during the copulatory

Herpetology Notes, volume 8: 15-18 (2015) (published online on 26 January 2015)

Corpse bride irresistible: a dead female tegu lizard(Salvator merianae) courted by males for two days

at an urban park in South-eastern Brazil

Ivan Sazima

Museu de Zoologia, Universidade Estadual de Campinas, 13083-970 Campinas, São Paulo, Brazil.

E-mail address: [email protected]

Page 2: Corpse bride irresistible: a dead female tegu lizard

Ivan Sazima16

attempts (Fig. a, c-e). These behaviours were displayed repeatedly during the time the males remained with the female. The smaller male briefly snorted twice during the copulatory attempts (no snorting was recorded for the larger male). This smaller male attempted to grab

the female’s hind and midbody (and even the tail), and sometimes rested on the carcass for periods of up to 4 min before resuming its courtship and mating attempts.

The common tegu is active from August to April in South-eastern Brazil (Andrade et al., 2004), and its

Figure 1. Necrophiliac behaviour of the common tegu (Salvator merianae) at an urban park in South-eastern Brazil: (a) mounted on a recently dead female, a large male gains hold biting the skin of her neck and attempts to mate; (b) the same male bites the female’s neck, while rubbing left hindlimbs on her body; (c) holding the same, now second day-dead and rotting female, a smaller male holds the skin of her neck and attempts to mate; (d) opening his jaws widely, the same male bites the female’s head; (e) the male rests on the carcass upon ceasing his attempts for a while; (f) shortly before leaving, the male tongue-flicked the female’s head and scratched her hindbody with the right hindlimb.

Page 3: Corpse bride irresistible: a dead female tegu lizard

Corpse bride irresistible: a dead female tegu lizard courted by males for two days 17

reproductive season begins about 1 month after the activity onset (Lopes and Abe, 1999), which is consistent with the observations reported herein. The courtship and mating attempts the males displayed in presence of the dead female are similar to those described by Lopes and Abe (1999) for live captive individuals. Snorting, a conspicuous behaviour during courtship and mating (Lopes and Abe, 1999), was almost absent from my observations.

Necrophiliac behaviour in teiids was recently recorded for Ameiva ameiva in South-eastern Brazil (Costa et al., 2010). These authors relate the courtship and mating attempts by males to the high temperature of the dead female, probably warm because of hers full exposition to sun in a dirty road at air temperature of about 33ºC. Thus, in the instances of necrophilia recorded for Ameiva and Salvator (Costa et al., 2010; present paper) air temperature was high and probably influenced the behaviour of the males.

Courtship and mating attempts by males in presence of freshly dead females (Costa et al., 2010; present paper) probably are related to sex pheromones still acting on the carcasses (Vitt, 2003). Since lizards are strongly influenced by pheromones during their sexual activity (Cooper et al., 1986; Cooper and Steele, 1997; Pianka and Vitt, 2003), males possibly were unable to perceive that the females they courted were dead. Additionally, male testosterone levels of the common tegu are highest after torpor emergence and at the onset of sexual interactions in September (Chamut et al., 2012). Female tegus are to a greater or lesser extent passive during courtship and copulation (Lopes and Abe, 1999), perhaps due to the larger size and strength of males, which also would partly explain the effort and time the males spent with a dead (thus, inert) female.

The second-day female carcass was no longer fresh and had a strong putrefying odour that attracted carrion-seeking flies. However, her odour notwithstanding, the bloated female was courted by a male. As tegus at the study site feed mostly on carrion (Sazima and D’Angelo, 2013), it is noteworthy that the male was sexually driven to this potential food source. One plausible explanation for this particular instance of necrophiliac behaviour is that sex pheromones still acted strongly on the carcass and overcame the putrefying odour, irrespective of strong innate prey odour discrimination displayed by tegus (Cruz-Neto and Andrade, 1993). Another plausible explanation is that the lesser tegu was younger and had less experience than the large male that courted the fresh carcass a day before. Whatever the cause, this seems the first record of a dead lizard female that

attracted different males for two consecutive days. The skink Tiliqua rugosa (Gray, 1825) forms a strong pair bond, and a male is recorded to tongue flick and nudge his female partner for a few days after her death (How and Bull, 1998), apparently responding to cues similar to those reported herein for the tegu lizard.

Acknowledgements. I thank to the staff of the Parque Ecológico Prof. Hermógenes de Freitas Leitão Filho for allowing field studies at the park; Marlies Sazima for her loving support; Ariovaldo P. Cruz-Neto for his thoughtful review; Alessandro R. Morais and an anonymous reviewer for helpful comments; the CNPq for earlier financial support.

References

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Accepted by Alessandro Morais

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