The Corpse Bride: A case of Davian behaviour in the Green Ameiva (Ameiva ameiva) in southeastern Brazil

Abstract

Herein, we report necrophilia (Davian behaviour) in the lizard Ameiva ameiva in Brazilian Atlantic Forest Domain. A male A. ameiva was found during a sunny day courting and trying to copulate with a road-killed female. The presence of developed ovarian follicles confirmed that the female was in breeding condition. The female probably died while making a chemical trail to attract reproductive males. Apparently the male’s behaviour was influenced by the high temperature of the female’s body that was warmed up by the heat of the sun. Although Davian behaviour is not expected to occur frequently, a high number of dead reproductive females in Brazilian roads could result in a high frequency of necrophilia in A. ameiva.

Full text

Introduction
Necrophilia has been reported in several species of
all major groups of tetrapods. There are observations of
this kind of behaviour in mammals (Dickerman, 1960;
Bagemihl, 1999), birds (Lehner, 1988; Moeliker, 2001;
Bagemihl, 1999), amphibians (Meshaka-Jr., 1996;
Bettaso, Haggarty and Russel, 2008; Sinovas, 2009)
and reptiles (Amaral, 1932; Belluomini and Hoge,
1957/1958; Lambiris, 1966; Sharrad, King and Cairney,
1995; How and Bull, 1998; Vitt, 2003; Fallahpour,
2005; Brinker and Bucklin, 2006). The name Davian
behaviour was rst used by Dickerman (1960) when he
observed necrophilia in ground squirrels Citellus (now
Spermophilus). The term is a reference to a limerick
about an old necrophiliac miner named Dave.
In the present work we describe courtship behaviour of
an adult male A. ameiva with a dead conspecic female
during eldwork in southeastern Brazil.
The Green Ameiva, Ameiva ameiva (Linnaeus,
1758) has one of the widest distributions among New
World tropical lizards, occurring in most of tropical
and subtropical South America on east of the Andes,
extending north to Panama (Vitt et al., 2008). This
heliothermic medium-sized teiid (snout-vent length
40-190 mm) inhabits a great number of ecosystems,
spanning from semi-arid regions to wet lowland forests,
and even habitats that are disturbed by human activity
(Vitt and Colli, 1994; Sartorius, Vitt and Colli, 1999).
Ameiva ameiva is sexually dimorphic, with adult males
being larger than females (Colli, 1991; Vitt and Colli,
1994; Rocha, 2008). Reproductive period varies along
a broad geographical range, tending to be continuous in
areas where rainfall is abundant throughout the year or
highly unpredictable, and cyclical in areas with a highly
seasonal climate (Colli, 1991; Vitt and Colli, 1994).
However, continuous reproduction has been reported in
Herpetology Notes, volume 3: 079-083 (2010) (published online on 23 March 2010)
The Corpse Bride: a case of Davian Behaviour in the Green Ameiva
(Ameiva ameiva) in southeastern Brazil
Henrique Caldeira Costa*1,2, Emanuel Teixeira da Silva1,2, Pollyanna Silva Campos3,
Marina Paula da Cunha Oliveira1, André Valle Nunes1 and Patrícia da Silva Santos4.
1 Museu de Zoologia João Moojen, Vila Gianetti 32, Univer-
sidade Federal de Viçosa, Viçosa, MG CEP: 36570-000,
Brazil; e-mail: ccostah@yahoo.com.br
2 Programa de Pós-graduação em Biologia Animal, Departa-
mento de Biologia Animal, Universidade Federal de Viçosa,
Viçosa, MG, Brazil;
3 Museu de História Natural Eduardo Marcelino Veado, Centro
Universitário de Caratinga – UNEC, Campus II, Rua Niteroi,
s/nº, Bairro das Graças, Caratinga, MG CEP 35300-000;
4 Pós-graduação em Ecologia Conservação e Manejo de Vida
Silvestre, Universidade Federal de Minas Gerais, Laboratório
de Herpetologia, sala 242 Bloco E2, Av. Antônio Carlos
6627, Pampulha, Belo Horizonte, MG CEP 31270-901,
Brazil.
* corresponding author
Abstract. Herein, we report necrophilia (Davian behaviour) in the lizard Ameiva ameiva in Brazilian Atlantic Forest Domain. A
male A. ameiva was found during a sunny day courting and trying to copulate with a road-killed female. The presence of developed
ovarian follicles conrmed that the female was in breeding condition. The female probably died while making a chemical trail
to attract reproductive males. Apparently the male’s behaviour was inuenced by the high temperature of the female’s body that
was warmed up by the heat of the sun. Although Davian behaviour is not expected to occur frequently, a high number of dead
reproductive females in Brazilian roads could result in a high frequency of necrophilia in A. ameiva.
Keywords. Squamata, Teiidae, courtship, necrophilia, reproduction.

Henrique Caldeira Costa et al.
80
habitats with marked seasonality (Rocha, 2008).
Despite the availability of biological data concerning its
reproduction, information on courtship and reproductive
behaviour of Ameiva ameiva remains scarce. To the best
of our knowledge, the only observations on A. ameiva
courtship in the wild were those presented by Manata
and Nascimento (2005) in Serra do Cipó National Park,
southeastern Brazil, and by Vitt (2003) at Amazon of
northern Brazil.
Materials and methods
Observations took place during an environmental impact as-
sessment on 12 March 2009, on a dirt road at the urban area of
the district of Tabajara, municipality of Inhapim, Atlantic Forest
of the state of Minas Gerais, southeastern Brazil (19.586500º S,
41.762614° W). There was herbaceous vegetation on one side of
the road, near a pen, and a house on the other side. Observations
were written down on a notebook, and some photos and videos
were taken using a digital camera (Sony DSC H 50).
Results
At 10:50 a.m. (air temperature ca. 33 ºC), we saw at a 5-
6 m distance, an adult male of Ameiva ameiva, mounted
on the back of a conspecifc dead adult female (probably
killed after being run over by a vehicle), on the centre
of the road. The male pressed his gular region against
her back, rubbed it repeatedly with lateral movements
of his head and icked tongue several times. Then, he
made a series of movements with his hind limbs, trying
to oppose his cloaca with the female’s (Fig. 1), but
apparently not everting his left or right hemipenis.
At 10:59 a.m. a second male, slightly smaller than
the rst one, came from the vegetation and began to
approach the female, being promptly chased away
by the rst male. Both males ran to the bushes close
to the road’s edge. At this time, the female’s tail lifted
up, and we checked to see if she was still alive (Fig.
2). After conrming it was dead, the female’s body was
returned to its former position. Soon after, the rst male
returned, circled around the female, and rubbed his
Figure 1. An adult male Ameiva ameiva courts a dead conspecic female (MZUFV 766). The male mounts on the back of the
female (A, B, C), and later makes series of movements with hind limbs, trying to pair his cloaca with the female’s (D, E, F). Photos
and video frames by E. T. da Silva.

Necrophilia in the Green Ameiva 81
Figure 2. A second male Ameiva ameiva, slightly smaller than the rst one, came from the vegetation and begins to get closer to
the female, being promptly frighten by the rst male (A-F). Both males ran to the bushes close to the edge of the road (G). At this
time, the female’s tail lifted up (H). Photo and video frames by E. T. da Silva.

head repeatedly, before attempting another courtship
engagement. The second male returned three more
times, only to be chased again by the rst one. Later,
the second male stayed around the area and crossed the
road.
A total of 11 charges of the rst male over the female
were observed, within 20 minutes since the beginning
of the observations. The last charge was at 11:09 a.m.,
and during the coupling trial the male went away from
the dead female twice, to short distances, still remaining
in the proximity of her body, without entering the
vegetation. After that, he abandoned the female’s body.
Eight minutes after the male left the scene, the female’s
body began to present signals of dehydratation. Her tail
was erect and head and front limbs were contracting. We
took the lizard from the road and collected it at 11:17
a.m. The two males were observed in close proximity
for ve more minutes, apparently foraging.
We interrupted the male’s behaviour ve times. In three
of them, we moved the female’s body away from the road
due to the passing of vehicles (returning it to the same
place soon after). Another time was for photographic
record, and the other was during the spontaneous lifting
of the female’s tail. There were also two voluntary
departures of the rst male besides the ones reported,
as a response to the second male’s approaches. In all
charges of the rst male over the female there were
coupling trials or courtship behaviour.
The dead female was xed in 10% formalin and
dissected, which revealed the presence of six apparently
fertilized eggs (14.1 x 12 mm; 14.45 x 12.35 mm; 14 x
13 mm; 14.65 x 12.5 mm; 15 x 12.2 mm; 14.7 x 12.75
mm) and several follicles in development (18 in the
right and 14 in the left ovary).
Discussion
Vitt (2003) was the rst to report necrophilia in
Ameiva ameiva, at Amazon biome in northern Brazil.
He shot a female that was being courted by a large male,
who instantly ran off. Soon after, the male returned,
tongue icked the area, located the female and tried
to mate with her, when he was shot. The same process
was done later with a second smaller male (Vitt, 2003).
Although the report of Vitt (2003) is quite similar to the
one presented here, the fact that he killed both males
soon after they tried to mate with the dead female did
not allow him make some behavioural observations (i.e.
the number and duration of coupling attempts or the
interactions between the larger and the smaller male).
The presence of ovarian follicles in development
shows that the dead female found by us was in breeding
season. Unfortunately, we do not know whether the rst
male was already courting the female when she was run
over, or if he rst found her only after she was killed. If
he was courting the female when she was killed (and he
luckily escaped), he just did not notice that his partner
was dead, continued the courtship and coupling trials,
like the case reported by Vitt (2003).
In both sexes of Ameiva ameiva, the ventral skin of
the thighs shows a single row of 16-23 femoral pores,
each one opening in the centre of a modied scale,
resembling a rosette (Imparato et al., 2007). As in other
lizard species, these pores are connected to internal
glands that produce a solid secretion containing non-
volatile chemical cues that play a relevant role in social
behaviour (Pianka and Vitt, 2003; Imparato et al., 2007).
Therefore, the female was probably secreting chemical
cues to attract breeding males to copulate. In A. ameiva
this method of signal dispersion is intimately dependent
on the locomotion, where the animal left a trail of
chemical signals on the substrate (Imparato et al., 2007).
Thus, the female could have been killed while engaged
in this behaviour.
The female’s chemical trail probably attracted both
male’s attention. The explanation for the males did
not know the female was dead might stand in the fact
that Ameiva ameiva is heliothermic, with relatively
high active body temperatures. Vitt and Colli (1994),
studying eight populations of A. ameiva in four Brazilian
biomes found that these lizards are active with body
temperatures from 26.4 to 42.2. ºC (mostly from 36 to
40 ºC). Observations reported here occurred during a
hot day, when the air temperature was at 33 ºC. This fact
may allow the body temperature of the dead female to
remain elevated, as she was directly exposed to sunlight,
in the centre of the dirt road, and this condition may
have confused the males.
If we are correct, special conditions may favour
necrophilia in Ameiva ameiva as a “behavioural
mistake”. In fact, this kind of mistake appears to
occur in several reports of animal necrophilia, when a
reproductive male tries to mate with a stationary and
seemingly “receptive” female (Lambiris, 1966; Lehner,
1988; Sharrad, King and Cairney, 1995; How and
Bull, 1998; Vitt, 2003; Fallahpour, 2005; Brinker and
Bucklin, 2006). In some cases, necrophilia can also be
just a result of a coupling trial by a male that usually
do not access partners carefully, a common behaviour
in some anurans (Meshaka-Jr., 1996; Bettaso, Haggarty
and Russel, 2008; Sinovas, 2009).
Henrique Caldeira Costa et al.
82

It is important to note that a high number of road killed
reproductive females of Ameiva ameiva possibly occur
along some Brazilian highways, especially in sunny
days and could even result in a high frequency of Davian
behaviour in this species, as reported for some explosive-
breeding anurans in United States (Meshaka-Jr., 1996).
However, the benets of being the rst to encounter a
female probably outweigh the costs of the mistakes that
can happen sometimes, like trying to couple with a dead
partner (Sinovas, 2009). It is possible that the impact of
Davian behaviour on the evolution of reproduction is
nonexistent (Sharrad, King and Cairney, 1995).
The female A. ameiva (135 mm. snout-vent length) is
deposited in the lizard collection of Museu de Zoologia
João Moojen, Universidade Federal de Viçosa, in
Viçosa, Minas Gerais, Brazil, under the label MZUFV
766.
Acknowledgments. We are grateful to Limiar Engenharia
Ambiental for nancial support and Instituto Brasileiro do
Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA)
for collection permits (#123/2009 NUFAS/MG; process
#02015.014980/2008-50) to ETS, PSC, MPCO, AVN and PSS;
Prof. Jorge Dergam for suggestions and English revision on an
early version of the manuscript; Prof. Izabel Maldonado for
identication of eggs and follicles; Carla S. Cassini, Kamelia
Algiers, Ligia Pizzatto and Walter E. Meshaka Jr. provided
essential bibliography. Prof. Eric R. Pianka suggested valuable
references and critically reviewed a rst draft of this paper. An
anonymous referee also made valuable suggestions on the nal
version of the text.
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