Intraspecific oophagy in Hierophis viridiflavus (Serpentes: Colubridae) during oviposition in a controlled environment

Abstract

Intraspecific oophagy in Hierophis viridiflavus (Serpentes: Colubridae) during oviposition in a controlled environment. Following the observation of adult pairs of the Western Whipsnake, Hierophis viridiflavus, in a controlled environment, two distinct but related phenomena were observed: egg deposition and predation of freshly laid eggs by the male. Data about deposition, number and morphology of the eggs, hatching and offspring are presented and compared with the literature. The episode of oophagy is described, confirming the inclination to predate snake eggs and intraspecific oophagy in this species.

Full text

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Phyllomedusa - 22(1), June 2023
PROOFS
Received 25 November 2022
Accepted 10 March 2023
Distributed June 2023
Intraspecic oophagy in Hierophis viridiavus
(Serpentes: Colubridae) during oviposition in a
controlled environment
Alessandro Paterna
OPHIS Museo Paleontologico e Centro Erpetologico, 64100 Teramo, Italy. E-mail: alessandro.paterna@hotmail.com.
Phyllomedusa 22(1):29–35, 2023
© 2023 Universidade de São Paulo - ESALQ
ISSN 1519-1397 (print) / ISSN 2316-9079 (online)
doi: http://dx.doi.org/10.11606/issn.2316-9079.v22i1p29-35
Abstract
Intraspecic oophagy in Hierophis viridiavus (Serpentes: Colubridae) during
oviposition in a controlled environment. Following the observation of adult pairs of the
Western Whipsnake, Hierophis viridiavus, in a controlled environment, two distinct but
related phenomena were observed: egg deposition and predation of freshly laid eggs by
the male. Data about deposition, number and morphology of the eggs, hatching and
ospring are presented and compared with the literature. The episode of oophagy is
described, conrming the inclination to predate snake eggs and intraspecic oophagy in
this species.
Keywords: Egg deposition, Intraspecic predation, Reproduction, Snakes, Western
Whipsnake.
Oofagia intraespecíca em Hierophis viridiavus (Serpentes: Colubridae) durante a ovipostura
em um ambiente controlado. Após a observação de pares adultos de cobra-chicote-do-oeste,
Hierophis viridiavus, em um ambiente controlado, dois fenômenos distintos, mas relacionados,
foram observados: deposição de ovos e predação pelo macho de ovos recém-depositados. Dados
sobre a ovipostura, o número e a morfologia dos ovos, a eclosão e os lhotes são apresentados e
comparados com os dados da literatura. O episódio de oofagia é descrito, conrmando a tendência
dessa espécie de predar ovos de serpentes e praticar a oofagia intraespecíca.
Palavras-chave: Cobra-chicote-do-oeste, Ovipostura, Predação intraespecíca, Reprodução,
Serpentes.
Introduction
Predation of bird eggs by snakes is
widespread in hundreds of species, especially
among colubrids (Schulz 1996). For most of
these, eggs and nestlings are part of a vast food
spectrum, while some species have a specialized
diet based on bird eggs (Gans 1959, Bates and
Broadley 2018).
Predation of reptile eggs by snakes is well
known, but observations in the wild in European
species are almost exclusively limited to the
predation of saurian eggs. This phenomenon has
been widely observed in Coronella austriaca
Laurenti, 1768 (Galán 1988, 1991, Galán and
Fernández Arias 1993, Amat 1998, Moreira et al.

30
Phyllomedusa - 22(1), June 2023
Paterna
2011, Lunghi et al. 2015, A. Paterna unpubl.
data), the congeneric Coronella girondica
(Daudin, 1803) (Luiselli et al. 2001), Zamenis
scalaris (Schinz, 1822) (Pleguezuelos et al.
2007), and the boid Eryx jaculus (Linnaeus,
1758) (Faraone et al. 2017). Data about predation
on reptile eggs in snakes arise mainly from the
dissection of roadkilled individuals or mani-
pulation of individuals in which regurgitation is
voluntarily or involuntarily induced.
Intraspecic oophagy in colubrids has been
conrmed almost exclusively in captivity (Mitchell
and Groves 1993), and the only European species
in which this phenomenon has been validated
with certainty is Z. scalaris (Laferrere 1970).
Snake egg predation has been reported in
Hierophis viridiavus (Lacépède, 1789). A
roadkilled adult male of this species that had
four snake eggs in its stomach and intestine was
found near a communal nesting site of the same
species (Capula and Luiselli 1995). The ingested
eggs were assumed to belong to the same species
of the predator. A similar case involving H.
viridiavus has been recently reported by Bonnet
et al. (2021) from western France.
The western whipsnake Hierophis viridiavus
is a colubrid snake widely distributed mainly in
Italy and southern France. Within this species,
two main phenotypes generally corresponding to
the two subspecies are present: the nominal
viridiavus, with a characteristic dorsal pattern
of yellow and black tones, and carbonarius, in
which the adult specimens exhibit melanism.
The northern apex of the distribution of this
species reaches the southern portion of the Metz
province, France, for viridiavus and the
southern Alpine arch for carbonarius (Kreiner
2007). Established populations outside their
natural distribution have been recorded in
western Switzerland in the Cantons of Vaud and
Valais (Meier et al. 2022). In 2017, a small
population of H. viridiavus was found in a
waste disposal area in southwestern Germany.
The origin of this allochthonous colony is
thought to have been the accidental introduction
of some individuals through waste delivery from
Italy, specically from the province of Napoli.
The local administration for the protection of
nature opted to capture as many specimens of H.
viridiavus as possible, providing private
breeders or organizations with the opportunity to
adopt the collected specimens (H. Laufer, pers.
comm.). This study is based on the data obtained
from observations of the captive specimens of H.
viridiavus originating from the allochthonous
colony and maintained at OPHIS Museo
Paleontologico e Centro Erpetologico.
Materials and Methods
Four specimens of Hierophis viridiavus
recovered by the company Büro für
Landschaftsökologie LAUFER (Oenburg,
Germany) were adopted and kept at OPHIS
Museo Paleontologico e Centro Erpetologico.
These individuals were captured on 12 and 13
April 2022 and delivered to OPHIS on 25 April
2022. After capture, the specimens were kept
separately. Two pairs were formed based on the
size of the specimens and housed in two
terrariums (100 × 60 × 50 cm) set up in a
“naturalistic” way, with branches, bark, plants,
and baltic peat as substrates. The snakes were
observed daily from their arrival at the
herpetological center to brumation (April–
October 2022). Weight of the snakes was
recorded periodically each month during their
activity period. Throughout the observation
period, the specimens refused any food that was
oered them, and they were force-fed every
seven days with thawed young Mus musculus
Linnaeus, 1758. After 47 days in captivity
oviposition occurred. Egg mass and size data
were collected using an electronic scale and
caliper, respectively. Eggs were transferred to an
incubator, built with insulating materials, and
warmed using an electronic thermostat and
further controlled by digital probes. The
incubator dimensions were 38 × 58 × 36 cm,
and within it, eggs were contained in two plastic
boxes (12 × 12 × 6 cm) with a transparent lid
and moist vermiculite as medium.

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Phyllomedusa - 22(1), June 2023
PROOFS
Intraspecic oophagy in Hierophis viridiavus
Results
Egg Deposition
Throughout the breeding period of the housed
specimens, there was a visible increase in the
mass of all individuals with the exception of one
male, which was distinguished from the
beginning by its larger size. The female who
shared the terrarium with this male molted on 31
May 2022. After this event, the possible presence
of eggs in the female was noticed, although no
copulation was observed. A closed container
measuring 27 × 18 × 8 cm, with a circular
entrance of 4 cm to allow the snake to enter, was
prepared with moistened vermiculite for possible
egg deposition.
On the morning of 13 June 2022, exactly
seven weeks after the arrival of the specimens at
the OPHIS Herpetological Centre, the female
began laying eggs not in the dedicated container,
but under bark that was used as a hiding place
(Figure 1). At 09:00 h her third egg was expelled.
Photographs were made quickly to minimize
disturbance. Two hours later, the female was in
the same position with eggs remaining inside
her, but the eggs that had been laid could not be
found. The terrarium, the nesting container, and
the entire substrate were searched, but no traces
of the eggs were found. The co-inhabitant male
was then removed from the terrarium to
determine if he had ingested the eggs. By
manipulation it was possible to make the male
regurgitate four intact eggs and one damaged
egg (Figure 2). These were cleaned and placed in
a separate container. The female was reintroduced
to the container dedicated to egg-laying inside
the terrarium, where, after ve hours from the
rst check, she laid three additional eggs. Two
days before egg deposition the female weighed
144 g; after oviposition she weighed 106 g.
Eggs
The clutch consisted of eight eggs. Three
were laid by the female in the appropriate
container (Figures 1 and 3A), while ve, of
which one was damaged, were recovered after
regurgitation by the male (Figure 2). Weight of
each egg was 6–7 g, lengths were 3.7–4.2 cm in
length, and diameter1.5 cm. The eggs were white
with a longitudinal striae-like pattern. Some eggs
exhibited asterisk-shaped concretions inside a
smooth circular recess that interrupted the rough
pattern of the surface (Figure 3).
The uneaten and regurgitated eggs were
placed in two separate containers with moist
Figure 1. Adult female Hierophis viridiflavus originating
from the southwestern Germany allochthonous
colony at the time of deposition at OPHIS
Museo Paleontologico e Centro Erpetologico.
Figure 2. Adult male Hierophis viridiflavus originating
from the southwestern Germany allochthonous
colony after regurgitating the eggs freshly
deposed by the conspecific female at OPHIS
Museo Paleontologico e Centro Erpetologico.

32
Phyllomedusa - 22(1), June 2023
vermiculite and placed inside the incubator at a
temperature between 25.5 and 27.5°C. Three
weeks after deposition, the regurgitated eggs
were removed from the incubator following
deterioration. This process was already evident
after a few days but was slowed, in vain, by
cleaning the surfaces of the eggs. During the
incubation period, the three remaining eggs
increased in size, expanding mainly transversally.
Hatch and Ospring
On the 56th day of incubation, two eggs were
cut, and the hatchlings (Figure 3B) emerged
from the eggs on the same day. The same was
done for the third specimen on the following
day. The hatchlings shed for the rst time eight
days following hatching. The hatchlings each
weighed 5 g and measured 28, 28.5, and 30 cm.
The male was the shortest and had the darkest
pattern (Figure 4). The head was black with
yellow lines; dorsum was greenish/grayish with
small darker rectangles. The chin was white,
fading to a light aqua-green on the ventral and
subcaudal scales. The iris was orange in contact
with the pupil, becoming darker at its outer edge.
Discussion
Reproduction
Information on the reproduction of Hierophis
viridiavus is plentiful in the literature. However,
in most sources, descriptions of the eggs, their
appearance, dimensions, and clutch size are
identical, without any specic data (Bologna et al.
2000, Vanni and Nistri 2006a, b). The only data
about gestation are found in Di Tizio et al. (2008),
where the authors stated that the time from mating
to egg-laying is 20–30 days. It is assumed that the
data concerning the reproduction of H. viridiavus
found in these sources, identical and non-specic,
all originated from Bruno (1984, 1998).
Original data on egg numbers are 5–10
(Luiselli 1995), 4–7 (Capula et al. 1997), 3–9
(Filippi et al. 2007), and 4–11 (Zu et al. 2007).
Figure 3. (A) Details of the last three eggs deposited by
the female Hierophis viridiflavus originating
from the southwestern Germany allochthonous
colony at OPHIS Museo Paleontologico e
Centro Erpetologico. (B) Hatching of two
Hierophis viridiflavus at OPHIS Museo
Paleon tologico e Centro Erpetologico. Clutch
laid by a female originating from the
southwestern Germany allochthonous colony.
A
B
Paterna

33
Phyllomedusa - 22(1), June 2023
PROOFS
Figure 4. Portrait of a male Hierophis viridiflavus
hatchling after its first shed at OPHIS Museo
Paleontologico e Centro Erpetologico. Hatched
from a clutch laid by a female originating
from the southwestern Germany allochthonous
colony.
Unfortunately, no information on morphology,
features of the eggs, or times and methods of
incubation were reported. Only two photos of
eggs or hatchlings have been reported (Ferri
1992, 1993, Ferri and Soccini 2002).
In the present study, it was not possible to
determine with certainty whether the fertilization
of the eggs occurred in the wild or in captivity,
as no copulation in captivity was observed.
Observation of copulation in the controlled
environment would have been dicult because
the snakes are extremely elusive and rarely
found outside their hiding places. The subjects in
this study came into contact with each other for
the rst time 47 days before deposition, the
earliest possible date on which the copulation in
captivity could have occurred. Gestations with
time frames identical to this have been observed
in Zamenis longissimus in three consecutive
years, where times of gestation were 48, 48, and
49 days, respectively (unpubl. data).
Egg-laying took place 13 days after the pre-
deposition molt and resulted in the female losing
just over 25% of her weight. The eggs were very
similar in appearance to those of the sympatric
Aesculapian snake Zamenis longissimus,
although smaller (up to 5.5 cm long and 2 cm
wide in Z. longissimus, personal observation).
The appearance and size of the hatchlings are
similar to those reported in a large number of H.
v. carbonarius from a communal nesting site in
Abruzzo (Paterna 2015).
Oophagy
Intraspecic oophagy in colubrids has been
conrmed almost exclusively in captivity
(Mitchell and Groves 1993), and the only
European species in which this phenomenon has
been documented with certainty is Zamenis
scalaris (Laferrere 1970). In the present study, it
was possible to document and conrm such
behavior as the predation of conspecic eggs in
Hierophis viridiavus because the event took
place in a controlled environment.
It is not known whether the instinct to
swallow eggs is aected by captivity, but the
male obviously recognized snake eggs as a food
item. To date, all specimens of H. viridiavus
housed at the OPHIS Herpetological Centre have
refused any food that has been oered to them
(mice, baby quails, baby rats, sh) and have
been force-fed for their sustenance. However,
when oviposition took place in this study, the
male found and swallowed the eggs in a short
time. This demonstration that the male did not
feed on the eggs randomly is conrmed by an
analogous event, also occurring in a controlled
environment, in a pair of H. viridiavus
carbonarius bred by researchers Tomaž Jagar
and Erika Ostanek in 2022 (personal
communication).
Adult H. viridiavus in nature have a very
broad food spectrum (Filippi et al. 2003, Lelièvre
et al. 2012, Mondino et al. 2022), although there
is no shortage of documented episodes of
ophiophagy (Capula et al. 2014) and cannibalism.
This broad food spectrum makes H. viridiavus
one of the most opportunistic European snakes
and may suggest that the males of the two above-
mentioned episodes likely fed on the eggs
produced by the co-occupying females
opportunistically, not distinguishing whether the
deposited eggs belonged to their own species or
Intraspecic oophagy in Hierophis viridiavus

34
Phyllomedusa - 22(1), June 2023
not. An alternative hypothesis is that the males
of this species are inclined to feed on the eggs of
conspecic females (where they come into
contact with them) for population control
purposes. Males of H. viridiavus are strongly
territorial, and predation on conspecic eggs
would reduce the number of rivals in the territory.
This also raises the question of whether H.
viridiavus could dierentiate its own eggs from
those of other conspecics and from other
sympatric species.
Moreover, it must always be considered that
the stimuli and stress to which these animals are
subject in the wild are completely dierent from
those in captivity, and, in the case of this species,
much of its ecology remains unknown. Further
investigations should be made in the future
because the impact of such behavior is potentially
inuential not only in the areas where the species
naturally occurs but also in introduced
populations, where the opportunistic nature of
the phenomenon could be interpreted as an
additional indication of the invasiveness of the
species in the allochthonous localities.
Acknowledgments
I thank the Associate Editor Ross D.
MacCulloch and the two anonymous reviewers
for their comments, wishes, and for improving
the manuscript, and the Editor-in-Chief Jaime
Bertoluci. I thank Hubert Laufer for the adoption
of the specimens of Hierophis viridiavus and
for personally delivering these animals to the
OPHIS Herpetological Center. I thank Tomaž
Jagar and Erika Ostanek for sharing their
experiences regarding the episode of intraspecic
oophagy that occurred in the pair of H.
viridiavus kept by them and for allowing me to
report it in this study.
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Editor: Ross D. MacCulloch
Intraspecic oophagy in Hierophis viridiavus