Ben-Gurion University of the Negev The Jacob Blaustein Institutes for Desert Research The Albert Katz International School for Desert Studies
The nocturnally-active Saharan sand viper, Cerastes vipera, is mainly a diurnal hunter
Thesis submitted in partial fulfillment of the requirements for the degree of "Master of Science"
By: Itay Tesler
March 2018
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Ben-Gurion University of the Negev The Jacob Blaustein Institutes for Desert Research The Albert Katz International School for Desert Studies
The nocturnally-active Saharan sand viper, Cerastes vipera, is mainly a diurnal hunter
Thesis submitted in partial fulfillment of the requirements for the degree of "Master of Science"
By: Itay Tesler
Under the Supervision of: Allan Degen, Jaim Sivan and Michael Kam
Wyler Department of Desert Agriculture
Author's Signature Date: 21.3.2018
Approved by the Supervisors Date: 21.3.2018
Approved by the Director of the School Date 21.3.2018
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The nocturnally-active Saharan sand viper, Cerastes vipera, is mainly a diurnal hunter Itay Tesler
Ben Gurion University of the Negev The Jacob Blaustein Institutes for Desert Research The Albert Katz International School for Desert Studies 2018
Abstract
Cerastes vipera is a small, nocturnally-active predator that captures its prey mainly by sit-
and-wait ambush. I hypothesized that the time of activity coincides with hunting and, consequently, predicted that C. vipera would prey primarily on nocturnal species. To test this prediction, I tracked these vipers to determine their time of movement and type of hunting mode and analyzed their fecal samples and regurgitated prey for dietary intake. Cerastes vipera started its active movement after sunset and terminated its movement prior to midnight, when it presumably selected a suitable site for sit-and-wait-ambush. The vipers remained in ambush position until mid-morning (~10:00) and averaged 10.0 ± 2.02 hours at their sit-and-wait position. Cerastes vipera fed mainly on diurnal Acanthodactylus spp. and, occasionally, on nocturnal lizards and, thus, our prediction was rejected. Adult C. vipera fed
primarily on adult Acanthodactylus spp. (45 of 47 lizards) but neonate C. vipera fed only on
neonate Acanthodactylus spp. (25 of 25 lizards). Based on feeding rates in free-ranging adult
C. vipera, I estimated that more than 78% of their prey was captured diurnally. Most
nocturnally-active lizards were captured by adult female vipers, demonstrating a sex-biased
hunting success at night. Sexual dimorphism is evident in C. vipera; besides being slightly
larger than males, females have pronounced black markings at the tip of their tails whereas
males do not. We suggest that females use caudal luring at night more effectively than do
males, enabling them to have better hunting success.
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Acknowledgements
I thank my supervisors Allan Degen, Jaim Sivan and Michael Kam for their patience, key
insights, long discussions and constructive criticism. I would also like to thank Sefi Horesh
for accompanying me on many field trips, sharing his data, and valuable discussions. I thank
Shlomo Hadad and Avi Rosenstrauch for their help and contributions to this research.
I also thank Boaz Shacham, my friend, and Yehudah Werner from the National
Natural History collections in the Hebrew University of Jerusalem for providing me with dry and preserved material and useful data for this study. I thank all my friends and volunteers who helped me in the field: David Azulai, Yonatan Vronsky, Asaf Appel, Udi Shani, Akiva
Topper, Tzoor Magen, Kesem Keses, Asaf Uzan, Hadas Boni, Erik Friedman and many others that I probably forgot unintentionally.
I would especially like to thank my late father, Moti, who motivated me to succeed and complete my studies; you will always be in my heart and my mother, Mali, for supporting me unconditionally through years of research and studies. Thanks to their support,
I was able to study and work in animal research and education, fields of great importance to me. Additionally, I would like to thank my siblings, Yael, Omri and Nir, and my aunt Ricky for supporting and motivating me throughout my years of studies.
Lastly, but most importantly, I would like to thank my wife Luna and our son Adam for putting up with the long nights I spent in the field, and some “surprises” in the refrigerator… I did not take it for granted.
Collection of animals and experimental procedures were done with permission from the Israeli Nature and National Parks Authority.
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Table of Contents EDIT PAGE NUMBERS
Title page …………………………………………………………….……………… 2 Abstract ……………………………………………………………….…………….. 3 Acknowledgements …………………………………………………….…………… 4 Table of Contents ……………………………………………………………………. 5 Introduction …………………………………………………………………………. 6 Materials and Methods ……………………………………………………………… 10 Study species ………………………………………………………… 10 Study Area …………………………………………………………… 11 Observations and data collection ……………………………………. 12 Diel activity of lizard species ……………………………………….. 13 Dietary fecal analysis ……………………………………………….. 13 Body condition ……………………………………………………… 16 Statistical methods …………………………………………………... 17 Results ………………………………………………………………………………. 18 Prey intake ………………………………………………………….. 20 Sit-and-wait ambush ……………………………………………….. 23 Discussion ………………………………………………………………….………. 27 Diurnal sit-and-wait hunting ………………………….……………. 28 Feeding rates, feeding times and fangs ……………………….….… 30 Caudal luring and sex-biased nocturnal hunting success …………… 32 Lizards vs rodents as potential prey ……………………….….……. 36 Prey size and intraspecific shifts in dietary habits …………………. 37 References ………………………………………………………………...………… 38 Appendix. Dichotomic key for identifying lizards based on their claw morphology 47
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Introduction
Predators employ two main hunting strategies to capture their prey: sit-and-wait ambushing and active hunting (Schoener 1971) although these strategies are considered two extremes of the spectrum (Miller, Ament & Schmitz 2013). Active hunters generally come in contact with prey items more often, but expend more energy in capturing prey (Scharf et al. 2006; Ross and Winterhalder 2015) and are more likely to be spotted by a predator, and thus have a higher risk of being captured than do sit-and-wait ambushers (Huey and Pianka 1981; Wall et al. 2013). Ambush predators invest much of their foraging behavior in seeking suitable sites to ensure hunting success. Both hunting strategies were found to be conserved phylogenetically in lizards and snakes (Wall et al. 2013), and both have their advantages.
Theoretical models have shown that it is more efficient to be a sit-and-wait predator than an active hunter if the prey is faster than the predator (Huey and Pianka 1981; Scharf et al 2006).
Consequently, sit-and-wait ambushing would be suitable for relatively slow moving snakes
(Goetz et al. 2016). This, indeed, is the case for the venomous Viperidae, as has been reported for the Great Basin rattlesnake (Crotalus oreganus lutosus; Glaudas et al. 2008), the
Asp viper (Vipera aspis; Naulleau and Bonnet 1995), and the Palestine saw-scale viper (Echis coloratus; Yosef and Zduniak 2015).
The Saharan sand viper, Cerastes vipera (Linnaeus 1758), the smallest known viper species (Horesh et al. 2017; Sivan et al. 2015), was classified as nocturnal (Werner 2016) and found to be nocturnally-active from sundown to mid-night (Sivan et al. 2013). It is mainly a sit-and-wait ambusher (Horesh et al. 2017). This viper can only hunt actively by entering the burrow of the prey, as this sidewinder moves too slowly to chase prey. It is hypothesized that the time of activity combined with the hunting strategy determines the potential type of prey consumed. Based on the diel activity of C. vipera and the coexisting lizard species (Fig. 1a), a simple model was constructed that combines its nocturnal activity time and sit-and-wait
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hunting strategy to predict its potential diet composition (Fig. 2). From this model, C. vipera
should capture mainly the nocturnally-active lizard species, Sphenops sepsoides and
Stenodactylus spp., when using sit and wait hunting and the diurnally-active lizards,
Acanthodactylus spp., when using active foraging. Sit-and-wait is the commonly used
hunting strategy of this small viper and is preferred on the basis of energy expenditure and risk taking. In the book ‘Reptile Life in the Land of Israel’, Werner (2016) reported that C. vipera preys on various lacertilians (lizards) during its nocturnal activity. However, the scant data available on dietary intake of C. vipera indicate that its main prey item is the diurnal
Acanthodactylus spp. (Heatwole and Davison 1976; Sivan et al. 2013). These seemingly
puzzling reports prompted this study.
The report by Heatwole and Davison (1976) was anecdotal and was based on fecal
analysis of only 3 individuals. In the report by Sivan et al. (2013), dietary intake was based
on snakes that regurgitated their prey, that is, on snakes that were observed shortly after
capturing prey at night, a rare observational event in field studies. Prey was identified in such
a manner for only 5.5% of 434 snakes that were captured. If, indeed, diurnal lizards comprise
the main prey item of C. vipera dietary intake, then active nocturnal hunting would be the
main mode of prey capture, and our initial observations (Sivan et al., 2013; Horesh et al.,
2017) and those of others (Heatwole and Davison 1976; Schnurrenberger 1959) that C. vipera
is mainly a sit-and-wait ambusher would be incorrect. How then can these contradicting
findings be explained? Or else, which of these scientific findings is wrong that may lead to
these conclusions?
Based on the viper’s nocturnal activity and mainly on a sit-and-wait hunting strategy
year-round, I predicted that its dietary intake would be mainly nocturnally-active species and
not as cited in the literature. In addition, since active hunting is considered more costly
energetically than sit-and-wait hunting, I predicted that it would be employed by individuals
7 with better body condition. To test these predictions, I determined dietary intake of free- living adult and neonate C. vipera of both sexes by fecal analysis, and their body composition from body mass and snout-vent length measurements. We also estimated the time of prey capture by these vipers.
Fig. 1a. Diel activity of Cerastes vipera and co-exsisting lizard species.
(A) Cerastes vipera, nocturnally active; (B) Acanthodactylus scutellatus, diurnally active, showing a bimodal activity pattern; (C) Acanthodactylus aegyptius, diurnally active, temporally separated from A. scutellatus by being active in the hotter hours of the day; (D) Sphenops sepsoides, nocturnally active; (E) Stenodactylus sthenodactylus, nocturnally active; (F) Stenodactylus petrii, nocturnally active; and (G) Scincus scincus, diurnally active.
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Fig. 1b. Lizard species found and photographed in our study area.
Hunting strategy Active hunting Sit-and-wait ambush Hunting time
Diurnal not applicable Acanthodactylus & Scincus
Nocturnal Acanthodactylus Sphenops & Stenodactylus
Fig. 2. Alternative scenarios for the preferred diet intake in free-living Cerastes vipera combining both hunting strategies and activity period. The arrows point in the direction of both expected decreased risk/cost and increased benefit between scenarios (see text for explanation).
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Materials and Methods
STUDY SPECIES
The Saharan sand viper or the Avicenna viper, Cerastes vipera (Linnaeus 1758) (previously named Aspis vipera; Schnurrenberger 1959), family Viperidae, the smallest known viperid
(Sivan et al. 2015), up to 35 cm, is distributed across northern Africa’s Saharan countries, the
Sinai Peninsula and, in Israel, across the western Negev (Werner 2016). It is nocturnally-
active, moves by sidewinding and is limited to sand and dune systems (Sivan et al. 2013;
Werner 2016). This viper is mainly a sit-and-wait predator (Horesh et al. 2017) that buries
itself below sand level when ambushing (Klemmer 1970; Sivan et al. 2013) but, occasionally,
employs active hunting (Horesh et al. 2017; Subach et al. 2009; Fig 3). This venomous snake
preys predominantly on lizards (Schnurrenberger 1959; Sivan et al. 2012; 2013; Subach et al.
2009).
Fig. 3. Cerastes vipera entering the burrow of Acanthodactylus spp. and, thus, employing active hunting strategy.
Cerastes vipera is active from spring to autumn (April to late October) and hibernates
during winter (November to late March). Prior to hibernation in November, it increases its
active hunting strategy, but this mode of prey capture is still employed considerably less than
sit-and-wait ambushing at this time (Horesh et al. 2017). Mating season is short, up to two
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weeks in early spring, from the end of April to the beginning of May, females are ovoviviparous and young appear in August. The female C. vipera is slightly larger than the male (Sivan et al. 2015), and the tip of its tail is black and conspicuously marked whereas that of the male is not, resulting in a sexual dichromatism that is apparent throughout ontogeny (Heatwole and Davison 1976; Kramer and Schnurrenberger 1963; Marx 1958).
STUDY AREA The study was conducted in the desert sand dunes surrounding Wadi Seher, Israel. Wadi
Seher is situated in the western Negev, 15 km south of Beer-Sheva (31° 48'N and 34° 54'E), at 320–340 m above sea level. The area has an annual average rainfall of 150 mm, all occurring in winter, mainly from November to March, with 60% falling in December and
January. The area is characterized by large annual variations in total rainfall and in its temporal and spatial distributions. Winters are mild - the coldest month, January, has mean minimum and maximum air temperatures of 7.6 and 18.1°C, respectively. Summers are hot and dry, lasting from June to September. The hottest month, August, has mean minimum and maximum air temperatures of 20.2 and 33.5oC, respectively. The dominant vegetation is of
the Saharo–Arabian type with the main plants in summer consisting of Artemisia monosperma, Stipagrosis scoparia, Convolvulus lanatus, Retama raetam, Stipa capensis,
Hammada scoparia, Neurada procumbes and Noaea mucronata (Sivan et al. 2013). The
research area was confined to a single dune, with low plant cover, and approximately 40,000
m2 (100 m x 400 m) in size. Six species of lizards were found in the research area: the diurnal
(1) Nidua fringe-fingered lizard (Acanthodactylus scutellatus) , (2) Egyptian fringe-fingered lizard (Acanthodactylus aegyptius) and (3), sandfish (Scincus scincus); and the nocturnal (4)
wedge snouted skink (Sphenops sepsoides); (5) Anderson’s short-fingered gecko
(Stenodactylus petrii); and (6) Lichtenstein’s short-fingered gecko (Stenodactylus sthenodactylus) (Sivan el al. 2012; Werner 2016; Fig 1b).
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Both Acanthodactylus and Stenodactylus dig burrows and remain within them during
their non-active diel phase (Werner 2016). However, only the burrows of Acanthodactylus stay open and, thus, allow active foraging by free-ranging C. vipera in search of prey (Horesh et al. 2017). It was possible to differentiate between burrows inhabited by neonate and adult
Acanthodactylus spp. because of the considerable difference in the size opening between them.
OBSERVATIONS AND DATA COLLECTION
Field research was done between spring (early April), when the snakes emerged from hibernation, and autumn (late October), 2017, when the snakes entered hibernation. The study area was searched for viper tracks for five to seven nights each month. Two people were able to cover the whole area by walking length-wise twice on the plot; distance between them was
20 m. When tracks (Fig. 3) were observed, they were followed from their source to the point where active movement ended for that night. In some cases, fecal samples were found along the trail of the snake. The location of these samples was recorded and the samples were later analyzed for prey consumed by the snake. Between 22:00 and 23:00, each snake was weighed to the nearest 0.01 g (O’haus Balance, Model CT 200) and measured for snout to vent length
(SVL) to the nearest 0.1 cm. Snakes were classified as neonates or adults on the basis of SVL and month of capture as suggested by Bonnet et al. (2011) for another snake species.
Individuals with a SVL < 15 cm were classified as neonates (1-2 months old, monitored in
August to October only) while those with a SVL > 15 cm were considered adults (> 1 year old, and included subadults) (Sivan et al. 2015).
The abdominal area of each snake was palpated gently and fecal material, when
present, was extracted manually from the snake by stroking its ventral side towards the
cloaca. Handling of the snake was completed within 4 minutes, and then the snake was released at the point of capture. Then, for approximately half of the adults and > 70% of the
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neonates, randomly chosen, monitoring continued and the location and position of the snakes
at the end of activity for that night were recorded, that is, sit-and-wait ambush or in a burrow/bush (Sivan et al. 2013). The tracks clearly indicated the final destination of the snake for that night. In July and August, six snakes (3 adult males, 1 adult female and 2 neonates) were chosen randomly from those that ended activity at a sit-and-wait position near a rodent/lizard burrow, and were observed till they terminated their ambush. To minimize disturbance, measurements on these snakes were taken at the end of the observation period.
In addition, we visited the study site at 05:30 am for another 4 days in an attempt to locate sit- and-wait C. vipera by following tracks and then observe their behavior during the day. Eight
C. vipera (5 adult males, 2 adult females and 1 neonate) were located and observed until they ended their ambush. These individuals had not been handled and behavioral data were used to support findings of nocturnally-tracked individuals.
DIEL ACTIVITY OF LIZARD SPECIES
In addition to literature reports on the activity time of the lizard species available at the study site, 4 transects, each of 100 m long and 0.5 m wide were examined for footprints of lizards
every 2 hours over 7 days in July. I was able to distinguish footprints at the genus level
between Acanthodactylus spp. and Stenodactylus spp., and identify S. sepsoides. Lizard
activity was measured as the average set of footprints, each related to an individual lizard, per
100 m transect per hour (FPH). Tracks which crossed the transect more than one time and
were obviously from one individual was only counted once. The FPH was assumed to
represent the relative abundance of these species/genus.
DIETARY FECAL ANALYSIS
Each fecal sample was air-dried and the content was spread in a Petri dish over 1 mm grid
paper to allow for size determination of the remains. Lizard plates, scales and claws were
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identified at a species/genus level and compared with these items in-situ. In addition, C.
vipera teeth and fangs were also found in fecal samples (Fig. 4d). Identification was made using a binocular microscope (Wild, model M7A, Heerbrugg, Switzerland) and was based on shape and size of the remains. Most samples contained one prey item; however some
contained two prey items. Diet composition of C. vipera determined by analyzing feces found on the ground, manually extracted fecal material, and regurgitated prey were combined.
Fig. 4a. Morphological comparison of lizard plates. (a) Adult S. sepsoides dorsal/caudal plate from feces; (B-C) Juvenile S. sepsoides dorsal/caudal plates from feces, note the dark margins on the plates; (L-Q) Adult S. sepsoides dorsal plate from preserved specimens; (M) S.sepsoides frontal plate from preserved specimen; (D-E) Frontal plates of adult and juvenile S. sepsoides from feces; (F-G) Frontal plates of adult and juvenile Acanthodactylus spp. from feces; (H) Caudal plate from adult Acanthodactylus spp. from feces; (J) Caudal plate from adult preserved A. scutellatus - note the median carinae; (I-K) Caudal plates from juvenile A. scutellatus from feces and preserved specimen, respectively; (O-P) Frontal and caudal plates, from preserved adult A. scutellatus; (N-R) Frontal and caudal plates, from preserved adult A.aegyptius; (S) Dorsal/caudal plates from juvenile Scincus scincus, from preserved specimen on the left, from feces on the right - note that there are no dark margins on the plates; (T-U) Head and caudal plates, of preserved adult S. sthenodactylus. Plates are presented on 1x1 mm paper. 14
Fig. 4b. A. scutellatus front (A) and hind (C) claws of a juvenile and hind (E and F) claws of an adult, A. aegyptius front (B) and hind (D) claws of a juvenile, S. petrii front (G) and hind (I) claws of an adult and S. sthenodactylus front (H) and hind (J) claws of an adult - all from preserved specimens. Drawings present specific morphological characteristics of Acanthodactylus spp. front (K and L) and hind (M and N) claws, and Stenodactylus spp. front (O and P) and hind (Q and R) claws. Plates are presented on 1x1 mm paper.
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Fig. 4c. S. scincus juvenile ventral (A) and dorsal (B) view of front claws. Adult S. sepsoides front (C) and hind (E) claws from feces and front (D) and hind (F) claws from preserved adult specimen. Drawings present specific morphological characteristics of S. scincus ventral (G), dorsal (H) and lateral (I) views of the claw, and ventral front (J), lateral front (K) and hind (L) and lateral hind (M) claws of S. sepsoides. Plates are on 1x1 mm paper.
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Fig. 4d. Lateral view of fangs (A) and regular teeth (B), and dorsal (C) and ventral (D) view of fangs of adult Cerastes vipera. ‘1’ and ‘2’ mark venom entrance orifice and discharge orifice. Fangs and regular teeth are from feces. Drawings present specific morphological characteristics of dorsal (E) and lateral (F) view of the fang and lateral view of a regular tooth (G). Plates are presented on a mm paper; each blue square is 1x1 mm.
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BODY CONDITION
Body condition index (BCI) is commonly calculated as a function of snout-vent length (SVL)
and body mass. In this study, we used the “scaled mass index” (Mi) to estimate body
condition in C. vipera, as has been done previously for this species (Sivan� et al. 2015). This
method uses the reduced major axis (RMA) for calculating a structural relationship. It has been shown to be a better predictor of variations in fat and protein reserves than other methods, including the residuals of the ordinary least squares intraspecific regression of body mass on SVL (see reviews and discussion in Peig and Green, 2009; 2010).
Calculation of BCI in the present study used equation 2 of Peig and Green (2009),
which took the form:
Mi = mbi RMA SVL0 b � �SVLi � where mbi and SVLi are the body mass and the snout to vent length of individual i,
respectively; bRMA is the scaling exponent estimated by the RMA regression of mb on SVL;
and SVLo is the arithmetic mean value for the study population. Statistical details for
calculating BCI in general were presented by Peig and Green (2009) while specific details for
C. vipera at the same research site were presented by Sivan et al (2015).
STATISTICAL METHODS
We did not scale-clip individuals for identification as we wanted to minimize the possible
effects of handling on the hunting strategy and behaviour of the snake. We have been
studying C. Vipera at this site for over 15 years (Sivan et al., 2012; 2013). In previous studies, it was reported that re-capture of marked individuals was very low (Horesh et al.
2017) and, therefore, pseudo-replications were minimal. Consequently, each point was considered as an independent measurement.
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Differences in body mass between C. vipera and lizard species found at the study site
were tested using one way ANOVA. Diel activity of lizard species/genus using FPH was
tested for interspecific differences using ANCOVA, taking the day and the transect as co-
factors. Wald statistic was used to determine significance of effects (Statistica 7.0, Stat Soft
Inc., USA). Chi square statistics were used to test whether age (neonates and adults) and sex
of C. vipera affected prey captured, fecal sample occurrence and behavior at the end of
nocturnal activity. Measurements are presented as means + S.D. and differences were
considered significant at p < 0.05 and as tended to be different at p < 0.10.
Results
In total, 161 adult (83 males and 78 females) and 52 neonate C. vipera (28 males and 24
females) were tracked and measured; adults were captured between April and October and
neonates between August and October. Samples for prey identification were obtained from
33% and 44% of adult males and females and 50% and 63% of neonate males and females,
respectively (Table 1). A significantly higher proportion of samples were collected from
2 neonates than adults (Chi (1) = 5.15, p = 0.025); there was no difference between male and
2 female adults (Chi (1) = 2.09, p = 0.148).
Body mass (mb) and snout to vent length (SVL) were greater in adults than in
neonates (Wald stats = 430.6 and 132.1, respectively), but were similar between snakes with
and without samples for prey identification (Table 1). Body condition index (BCI) was
similar (Main effect ANOVA) between males and females (16.8 ± 0.48 and 16.5 ± 0.41;
F(1,168) = 0.116 ; p = 0.73), and between adults and neonates (16.4 ±0.36 and 17.2 ± 0.60;
F(1,168) = 1.155 ; p = 0.28). It was also similar (ANOVA) between C. vipera which provided samples for prey identification and those which did not (16.8 ±0.43 and 16.5 ± 0.43; F(1,172)
= 0.180 ; p = 0.67). However, mean BCI was higher in individuals with samples than those
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without samples in neonates (18.0 ±0.70 and 15.5 ± 1.01; F(1,42) = 4.338; p = 0.043), and
was higher in neonates than in male adults with fecal samples (19.7 ±1.24 and 15.2 ± 0.52;
F(1,34) = 14.41; p < 0.001) (Table 1).The mb and SVL were significantly greater in adult C. vipera (19.9 ± 7.62 g and 216 ± 38.1 mm) than in six adult lizard species and were also
greater in neonate C. vipera (4.7 ± 1.90 g and 135 ± 19.1 mm) than in the six neonate lizards
occupying the study site (Table 2).
Table 1. Number of C. vipera with or without prey sample (fecal, manually extracted and regurgitated samples), and their mean (± SE) body masses, snout to vent lengths (SVL) and body condition indices (BCI).
Adults Neonates Males Females Males Females Number 83 78 28 24 With sample 27 (32.5%) 34 (43.6%) 14 (50.0%) 15 (62.5%) Body mass (g) 17.8 ± 0.94 27.9 ± 4.23 4.6 ± 0.47 4.5 ± 0.56 SVL (mm) 219 ± 4.7 226 ± 4.0 130 ± 5.1 134 ± 3.8 BCI 15.2 ± 0.52 16.4 ± 0.76 19.7± 1.24 16.7 ± 0.99
Without sample 56 (67.5%) 44 (56.4%) 14 (50.0%) 9 (37.5%) Body mass (g) 17.9 ± 0.74 21.8 ± 1.61 4.1 ± 0.60 5.8 ± 0.61 SVL (mm) 212 ± 6.2 211 ± 8.9 130 ± 7.2 154 ± 6.0 BCI 16.6 ± 0.84 16.9 ± 0.66 16.3 ± 1.13 14.6 ± 0.88
Table 2. Snout to vent length (SVL) and body mass (±SD) of free-ranging C. vipera (161 adults and 52 neonates), and six lizard species (n = 5 for adults and neonates of each species) at the study site.
Species occupying the study site SVL (mm) Body mass (g) Age Adults Neonates Adults Neonates Cerastes vipera 216 ± 38.1 135 ± 19.1 19.9 ± 7.62 4.7 ± 1.90
Diurnal lizards: Acanthodactylus scutellatus 53.4 ± 9.66 34.3 ± 6.03 5.9 ± 2.48 1.0 ± 0.58 Acanthodactylus aegyptius 50.0 31.8 ± 2.17 3.5 0.7 ± 0.16 Scincus scincus 85.8 ± 2.17 43.7 ± 1.53 17.4 ± 2.17 1.9 ± 0.08 Nocturnal lizards Sphenops sepsoides 71.2 ± 10.85 32.5 ± 3.54 4.8 ± 0.73 0.9 ± 0.13 Stenodactylus petrii 67.5 ± 18.48 30.0 ± 0.82 6.2 ± 0.95 0.6 ± 0.05 Stenodactylus stenodactylus 50.8 ± 9.23 22.0 ± 6.56 3.8 ± 0.35 0.5 ± 0.24
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The number of footprints per hour (FPH) differed among lizard species (Wald stat. =
42.20; p<0.001); effects of transect (Wald stat. = 0.108; p=0.74) and day (Wald stat. = 3.148; p=0.076) were insignificant. The 12.8 ± 0.05 FPH of Acanthodactylus spp., observed only
during daylight, were significantly higher (Wald stat. = 23.00; p<0.001) than the 1.68 ± 0.373
FPH of S. sepsoides and the 0.86 ± 0.734 FPH of Stenodactylus spp., observed only during
dark hours. The FPH of S. sepsoides was higher (Wald stat. = 4.98; p=0.026) than that of
Stenodactylus spp.
PREY INTAKE
To determine whether prey consumed could be identified by fecal analysis, 5 C. vipera were
offered either Acanthodactylus spp. or Stenodactylus spp., feces were collected and scales,
claws and teeth in the fecal samples were compared with those of the prey. No difference was
found between the items from the live specimen and in feces. Overall, 61 and 29 samples
from adults and neonates, respectively, were analyzed for prey identification. (Table 1). Of
these samples, 36 from adults (17 males and 19 females) and 7 from neonates (4 males and 3
females) were collected as defecated samples along the trail of the snake (e.g., Fig. 5).
Consequently, of the total number of C. vipera, 22.4% and 13.5% of adults and neonates,
respectively, defecated naturally. The distance between the night shelter of the snake and the
fecal sample ranged widely, between 10 cm and 22 m and averaged 5.8± 7.45 m and 4.1±
4.91 m in adult males and females, respectively, and 15 ± 7.1 cm and 64 ± 77.3 cm in neonate
males and females, respectively. Five adult C. vipera regurgitated their prey while being
handled and, therefore, had recently captured it (1 female and 1 male consumed
Stenodactylus spp, 1 female and 1 male consumed Acanthodactylus spp and 1 female
consumed S. sepsoides). Similarily, 3 neonates regurgitated their prey (2 males consumed
Acanthodactylus spp. and 1 female consumed Stenodactylus spp.).
21
Fig. 5. Fecal dropping of free-ranging Cerastes vipera and specific identification traces; before defecation, during defecation, and moving after defecation.
Items found in each fecal sample were remains (Fig. 4) of at least one lizard species/genera of either Acanthodactylus spp., S. sepsoides, S. scincus or Stenodactylus spp.,
C. vipera teeth and some insect remains, presumably from the lizards’ digesta. Differences between the two Acanthodactylus species could not be distinguished and neither could differences between the two Stenodactylus species and, therefore, were identified as either
Acanthodactylus spp. or Stenodactylus spp. Differences in shape or dimensions of either claws and scales among the four lizard species/genera and/or C. vipera rear teeth and fangs were significant (Table 3; Fig. 4), which permitted the identification of one or two prey species in each sample analyzed. Also, all parameters measured in situ between neonates and adults of each lizard species differed significantly (p < 0.01).
22
Table 3. length (mm; ± SD) of items within C. vipera fecal sample and comparison with similar items from actual specimen (n=5). Lizard species Adults Neonates In situ In feces In situ In feces Acanthodactylus spp. Frontal scale 4.4 ± 0.45 4.4 ± 0.25 2.6 ±0.10 2.6 ± 0.14 Caudal scale 1.3 ± 0.16 1.4 ± 0.08 0.6 ± 0.17 0.7 ± 0.08 Front leg claw 1.8 ± 0.19 1.9 ± 0.10 1.1 ± 0.12 1.0 ± 0.10 Rear leg claw 2.7 ± 0.25 2.7 ± 0.22 1.5 ± 0.18 1.4 ± 0.21
Scincus scincus Caudal scale - - - 1.7 ± 0.11 Front leg claw - - - 1.7 ± 0.17
Sphenops sepsoides Frontal scale 3.5 ± 0.36 3.7 ± 0.25 2.3 ± 0.15 2.2 Caudal scale 2.0 ± 0.25 2.0 ± 0.13 0.9 ± 0.18 0.8 ± 0.05
Front leg claw 0.6 ± 0.20 0.6 ± 0.13 0.2 ± 0.06 NA Rear leg claw 1.1 ± 0.17 1.2 ± 0.14 0.5 ± 0.11 NA
Stenodactylus spp. Head scale 1.4 ± 0.54 NA NA NA Front leg claw 1.5 ± 0.20 1.7 ± 0.15 NA NA Rear leg claw 1.6 ± 0.13 1.6 ± 0.17 NA NA
C. vipera Fang - 2.97 ± 0.206 - 1.90 ± 0.200 Rear teeth - 0.55 ± 0.107 - 0.30 ± 0.058
We were able to detect 2 prey items within a single fecal sample in 12 cases, 13% of all samples; all contained at least one Acanthodactylus spp. Four of these had a second
Acanthodactylus spp., while six contained S. sepsoides, one contained Scincus scincus, and one contained Stenodactylus spp. Overall, 47 Acanthodactylus spp., 15 S. sepsoides, 4
Stenodactylus spp. and 1 S. scincus were identified in adult samples, and 27 Acanthodactylus spp., 1 S. sepsoides and 1 Stenodactylus spp. were identified in neonate samples (Table 4).
23
Table 4. Diet composition in adults and neonates, males and females, based on fecal analyses.
Prey Prey activity Adults Neonates Males Females Males Females Acanthodactylus spp. Diurnal 23 24 13 14 Scincus scincus Diurnal 0 1 0 0 Sphenops sepsoides Nocturnal 2 13 1 0 Stenodactylus spp. Nocturnal 2 2 0 1
Of the 47 Acanthodactylus spp.consumed by adult C. vipera, only two were neonates,
while all 27 Acanthodactylus spp. consumed by neonate C. vipera were neonates. For
statistical analyses, we compared snakes that consumed nocturnally-active lizards (S.
sepsoides and Stenodactylus spp.) with snakes that consumed diurnally active lizards
(Acanthodactylus spp. and S. scincus). Snakes with samples containing both nocturnally and
diurnally active lizard species (N = 7) were included in the snakes consuming nocturnally
active lizard species, and, thus, there was a slight over estimation of the snakes capturing
nocturnally-active lizards. A significantly higher proportion of adults consumed nocturnally-
2 active prey species than did neonates (31.1% vs 7.1%; Chi (1) = 5.45, p = 0.020); the difference remained significant with adults examined only during August – October when
2 neonates were captured (Chi (1) = 4.16, p = 0.041). Within adults, a higher proportion of
2 females than males (44.1 % vs 14.8%) consumed nocturnally-active lizards (Chi (1) = 6.03, p
= 0.014). Even when tested among prey items, there was a significantly higher proportion of
2 nocturnally-active prey species consumed by females than by males (Chi (1) = 4.08, p =
0.043). Size (SVL; 22.6 ± 0.71 cm) and body condition (BCI; 16.3 ± 1.28) of females
consuming nocturnal lizards were similar to both females (SVL: 22.7 ± 0.44 cm and BCI:
16.6 ± 0.87) and males consuming diurnally-active lizards (SVL: 21.5 ± 0.51 and BCI: 15.5 ±
0.63). Overall, dietary intakes of adult males and neonates of both sexes contained less than
15% nocturnally-active lizard species, whereas that of adult females contained more than
37% nocturnally-active lizard species, that is, proportionally more than double the number. In
24
addition, 1 to 3 C. vipera fangs were found in 11 and 3 samples in adults and neonates,
respectively, and 2 to 25 C. vipera regular teeth were found in 11 and 6 samples in adults and neonates, respectively (Table 5). Ten of the samples containing fangs (71.4%) were from natural defecation, which comprised 23% of these samples.
Table 5. Sample size, fangs and teeth in C. vipera fecal samples. Values are means ± SD.
Item Adults Neonates Males Females Males Females Sample size 6 (24%) 5 (14%) 1 (7%) 2 (13%) Number fangs 2.0 ± 0.63 1.4 ± 0.54 3 1.5 ± 0.71
Sample size 5 (9%) 6 (14%) 3 (21%) 3 (33%) Number rear teeth 10.8 ± 6.18 6.0 ± 9.34 2.0 ± 0.58 2.0 ± 1.55
SIT-AND-WAIT AMBUSH
Overall, 86 adult and 43 neonate C. vipera were tracked during their nocturnal activity that
ended between 11:00 and 12:00 midnight, at which time 46 (53%) adults and 22 (51%) neonates ended their activity in a sit-and-wait hunting position in front of a bush or a burrow opening. The other C. vipera ended nocturnal activity within a rodent burrow or inside a
2 2 bush. This behavior was similar between sexes (Chi (1) = 0.21, p = 0.643 and Chi (1) = 0.024,
p = 0.876, in adults and neonates, respectively) and similar between adults and neonates
2 (Chi (1) = 0.06, p = 0.803). Also, BCI was similar between C. vipera that ended or did not end
their activity in a sit-and-wait position (16.8 ±0.60 and 15.7 ± 0.44; Wald X²(1) = 2.108,
p=.147).
25
Fig. 6. A female Cerastes vipera submerged in the sand (eyes are seen at the surface level; 1) at a sit-and-wait ambush position near fresh Stenoductylus spp. feces; (2) foot prints of the lizard, Stenodactylus spp.; 3), the blackened tip of Cerastes vipera tail start wriggling (leaving marks on the sandy surface; 4) performing caudal luring.
All C. vipera at a sit-and-wait hunting position were buried in the sand. While ambushing, adult females wriggled the tip of their tail above ground in a typical behavior
(Fig. 6); this behavior was never observed in males. The tip of the female tail had black markings but that of the male did not. Sit-and-wait ambush was found either in front of a burrow opening (of a rodent or Acanthodactylus spp.), in front of a bush, near lizard feces, or in the open dune. On several occasions we noticed adult gerbils of either Gerbillus pyramidum or Gerbillus alenbyii exhibiting behaviours such as sand kicks or close approach and jump backs when the viper was in a sit-and-wait ambush in front of their burrow openings. The C. vipera would then leave its ambush position and move to a different location. For statistical purposes, we combined all ambushing in front of a burrow opening for comparison with all other ambush sites. Of the 46 and 22 adults and neonates, respectively, in a sit-and-wait ambush, there was no significant difference between sexes
26
2 2 (Chi (1) = 1.08, p = 0.300 and Chi (1) = 0.73, p = 0.392, in adults and neonates, respectively),
but a higher proportion of adults tended to ambush near a rodent burrow than did neonates
2 (Chi (1) = 3.24, p = 0.072). For sit-and-wait ambush, in front of a rodent burrow was most common in adults, but least common in neonates (Table 6). Furthermore, adult C. vipera females were not observed in sit-and-wait ambush in front of a burrow opening of
Acanthodactylus spp., which was in contrast to adult males and neonates of both sexes, where relatively high proportions did so.
Table 6. Behavior of free-ranging C. vipera at the end of their nocturnal activity and the average distance (±SD) to either Acanthodactylus burrow opening, a rodent burrow opening or a bush, when at sit-and-wait ambush position. Percentage of sit-and-wait position within a column group is in brackets.
End of nocturnal movements Adults Neonates Males Females Males Females In a rodent burrow 2 4 1 0 In a lizard burrow 1 5 2 1 In a bush 15 13 8 9 At a sit-and-wait ambush position 23 23 11 11
Sit-and-wait ambush sites: In front of a burrow opening of a rodent 13 (57%) 16 (70%) 1 (9%) 1 (9%) Distance from opening (cm) 24 ± 12.7 28 ± 15.5 of Acanthodactylus spp. 6 (26%) 0 (0%) 6 (55%) 4 (36%) Distance from opening (cm) 3.0 ± 1.73 - 4.7 ± 4.62 3.5 ± 0.71 In front of Stenodactylus droppings 0 (0%) 0 (0%) 1 (9%) 1 (9%) In front of a bush 2 (9%) 6 (26%) 2 (18%) 1 (9%) Distance from bush (cm) - 40 ± 20.0 - - In the open 2 (9%) 1 (4%) 1 (9%) 4 (36%)
When in sit-and-wait ambush in front of an Acanthodactylus burrow opening, both
adult and neonate C. vipera were found at similar distances from the burrow opening, usually
within a few centimeters. However, neonates ambushed in front of neonate Acanthodactylus
burrows, whereas adult C. vipera males ambushed mainly in front of adult Acanthodactylus
burrows. Adults at sit-and-wait ambush in front of a rodent burrow or a bush were at a further
27
distance than when in front of a Acanthodactylus burrow opening, averaging between 20 and
40 cm (Table 6; Fig. 7).
Fig. 7. An adult Cerastes vipera at a sit-and-wait ambush position facing a burrow of an adult Acanthodactylus spp.
The six snakes that were observed throughout their nocturnal activity till after sunrise
remained at their sit-and-wait ambush position until mid-morning (~10:00), at which time
they left their ambush site, moved into the opening of the burrow and crawled inside. These
snakes remained at their sit-and-wait ambush position for 10.0 ± 2.02 hours. The snakes
stayed in their burrows till after sunset, after which time they emerged from their burrows and
started their activity. The eight snakes that were observed (5 adult males, 2 adult females and
1 neonate) at about 6:00 am in a sit-and-wait position facing an opening all entered a burrow
at about 10:00 (Fig. 8).
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Fig. 8. Two Cerastes vipera (inside dashed circles) burrowed in diurnal ambush position at 10:00 AM. (A) rodent burrow; (B) lizard burrow.
Discussion
Based on the activity period of C. vipera and their mode of sit-and-wait hunting strategy, we
predicted that these snakes would consume mainly nocturnal lizards. However, 75 of 96 prey items (78%) were diurnally-active lizards, and, therefore, our prediction was rejected. Adult female C. vipera consumed the highest proportion of nocturnal lizards, 15 of 40 prey items, but they too did not support our prediction. Consequently, our main hypothesis that activity time reflects the type of prey captured was not supported. Acanthodactylus spp., the most abundant lizards at the study site, comprised most of the dietary intake of C. vipera, which is in agreement with other studies that reported on prey items consumed by C. vipera (Arbel
1984; Heatwole and Davison 1976; Sivan et al. 2013; Subach et al. 2009).
29
DIURNAL SIT-AND-WAIT HUNTING
The choice between sit-and-wait ambush and active hunting has been studied in many
predator species. When the escape speed of the prey exceeds the predator speed, sit-and-wait strategy is optimal and preferred (Ross and Winterhalder 2015; Scharf et al. 2006) but requires extremely fast strike action. Indeed, within Viperidae, snakes having very long fangs and extremely fast striking speed (Cundall 2009; Higham et al. 2017), it is the most common hunting strategy (Rabatsky and Farrell 1996), as was reported also for C. vipera (Horesh
2017). Activity of ambushers would then be spent mainly in the search of suitable ambush sites (Clark et al. 2016; Goetz et al. 2016). Some vipers spend long periods of time in ambush that can last many hours and even up to several days in sit-and-wait position (Clark et al.
2016, Greene and Santana 1983; Reinart et al. 1984; Tsairi and Bouskila 2004). This is possible as their ambush sites are generally protected from high solar radiation, for example, within a tree canopy (Yosef et al. 2012) or on the ground under shaded areas or under boulders or logs (Tsairi and Bouskila 2004). However, this is not the case for C. vipera that
ambushes in an open area buried under sand. Consequently, C. vipera must leave its ambush
site before noon and find shelter within burrows or under bushes (Schnurrenberger 1959;
Werner 2016) to escape the harsh heat, which limits the time frame in which C. vipera can
capture its prey. In this study, approximately half of the vipers were in a sit-and-wait ambush position at the end of their nocturnal activity, starting about midnight and lasting till at least dawn.
It was previously suggested that diurnally-active Acanthodactylus spp. are
preferentially predated by C. vipera simply because they are the most abundant lizards in the
area (Heatwole and Davison 1976). This was also the situation in our research site, but while
population density of the prey might be one of the preliminary evolutionary triggers, we still
need a more comprehensive explanation for this phenomenon which would take into account
30
the major hunting strategy of the snake and difference in diel activities. my hypothesis was based on the premise that times of activity is associated with hunting times, and the available
prey within each diel phase. However, only about 25% of prey was captured at night.
Reasoning that most individuals were feeding on diurnally-active lizards and were using
mainly sit-and-wait as a preferred hunting strategy year round, i propose a new outlook on the
hunting strategy of C. vipera.
I hypothesize that their activity at night does not reflect hunting time but rather the
search for a suitable sit-and-wait ambush site for the diurnal Acanthodactylus spp. The
ambush at times when their potential prey is not active decreases chances of being exposed to
the prey, as was suggested by Downes and Shine (1998). Support for this hypothesis was that
a high proportion of C. vipera were in a sit-and-wait position at about mid-night in front of
rodents and Acanthodactylus spp. burrow openings and remained there till late morning
(Fig.8). Consequently, a sit-and-wait ambusher at night would have the chance to capture
nocturnally-active lizards based on their spatial distribution and foraging tactics and the
hunting success of the predator; this occurred in 28.4% and 6.9% of the cases in adults and
neonates, respectively.
During this study, I did not record an actual capture of prey during light hours.
However, on two occasions (at 9:00 am on 2nd July 1996 and 10:00 am on 5th September
2002), I observed the capture of adult Acanthodactylus scutellatus by adult male C. vipera
(I.T., unpublished data). The strike and predation were in front of a rodent burrow opening, and shortly afterwards, the snakes entered into the burrow with their prey. These anecdotal
observations are meaningful in light of our new hypothesis. Such sightings are only few,
possibly due to the fact that most studies on C. vipera are done at night.
31
FEEDING RATES, FEEDING TIMES AND FANGS
Feeding rate is not easy to determine in the wild, especially in snakes. However, if we assume
an ideal random distribution of feeding interval and food passage time among proportion of
individuals, than the natural fecal droppings are indicative of feeding rates. Natural fecal droppings were found for 22.4% of adults in this study, which implies an estimated average feeding rate interval of four to five days. The proportion of natural fecal samples in neonates was smaller, comprising 13.5% of neonates in this study, which may indicate a longer period between prey capture and a feeding rate interval of every 7 days.
Furthermore, as only 3.1% of total adults (n = 5) in the present study were found
shortly after hunting a prey at night, than 13.8% , of the population was estimated to feed
nocturnally and 86.2% hunted diurnally. In other words, whereas 3.1% were estimated to
feed nocturnally, 20.6% were estimated to feed diurnally. In a previous study, at the same
research site on free-ranging C. vipera spanning over 15 years, 5.5% of the overall population
(24 /434 individuals; Sivan et al. 2013) fed on nocturnally-active prey. Based on similar
considerations as above, 77% of the population consumed diurnally-active prey. Both of
these estimates are similar and further support our conclusions that the nocturnally-active C.
vipera is mainly a diurnal hunter.
C. vipera fangs and regular teeth were found mainly in the naturally-defecated feces,
in almost a quarter of these samples. Envenomation and functional limitation of fangs are
important for a successful strike (Cundall 2009) and the loss of fangs needs clarification.
Fangs are special maxillae teeth containing either a superficial groove or an enclosed canal
(as in Elapidae and Viperidae) along which the venom runs. Viperid snakes have the longest
fangs of all snakes and are equipped with a complex anatomical configuration allowing the
fangs, when not in use, to fold back via a rotating maxilla.
32
The development of fangs (e.g., Klauber 1939; Tomes 1877; Zaharandicek, Horacek
& Ticker 2008) and envenomation function (e.g., Cundall 2002; 2009; Higham et al. 2017) have been studied and documented many years ago. Extreme fangs are fragile, can easily break or wear out and, therefore, must be replaced regularly. Based on earlier suggestions
(Tomes 1877) Klauber (1939) was the first to reveal that there are two sockets used alternately to hold the active fang at each maxillae; the immature fangs in different developmental stages are contained in a magazine in a staggered line behind the two sockets
(e.g., Fig 18 in Klauber 1939; Fig 1E in Zaharandicek, Horacek & Ticker 2008). The active fang is replaced periodically in the vacant socket, alternatively in the inside and the outside positions, and a-synchronically for the two fangs on both sides. As fangs are essential, the active fang does not fall off (unless damaged) naturally before the replacement fang takes place. Consequently, on the day of replacement and for some time, both sockets on either the right or the left side are occupied and the viperid has 3 functional fangs (e.g., Fig. 7.18 in
Berkowitz & Shellis 2015).
Interestingly, fang replacement is not mentioned when studying limitations of viper fangs (Cundall 2009) and fang replacement rate is not documented. We found only two anecdotal mentions on the the replacement period of fangs; either every month or every two months, but even then, no details concerning data sources were available.
When hunting, venomous snakes may strike, release the prey, and then follow the trail to the dead victim or strike and hold the prey until paralyzed, as is the case with viperids hunting birds (i.g. Fathinia et al 2015). Viperid snakes usually strike and release the prey., ,
Cerastes vipera, however, hold their prey for several minutes after striking during which time the prey struggle to free themselves (personal observation). This process may result in the dislodging of fangs and regular teeth. These teeth are found mainly in naturally defecated samples; samples extracted manually were much smaller and could possibly be sub-sample
33
remains. However if their occurrence is indicative of replacement rate, then C. vipera requires a new pair of fangs twice each month. The present study is the first quantitative
report of fang loss and its excretion in a free-ranging viperid.
In general, and especially in free-ranging C. vipera, fangs seems to be an expensive resource. As they are found in 25% of the naturally defecated fecal samples, it is estimated that some fangs are lost for at least every four prey captured. Since feeding rate is estimated as four days, losing fangs occurs at least twice monthly on the average. Furthermore, as more
than one fang is lost each time, we reasoned that fang loss occurs before the fang is naturally
replaced. Fang length in viperid snakes is related to snake length (Klauber 1939) and thus, the
relatively high rate of fang loss in this small viper is in accordance with the prediction that
smaller fangs are more fragile than larger fangs. It follows that fang management in free-
ranging C. vipera could be handled via a faster than expected replacement period or,
alternatively, the snake is forced to stay in shelter and delay predation, thus avoid hunting at
times when fangs are absent. Further assessment of these costs due to rapid fang loss could be
estimated when more data become available on fang replacement rate among other viperids.
CAUDAL LURING AND SEX-BIASED NOCTURNAL HUNTING SUCCESS
A sit-and-wait ambusher is dependent on prey movements for encounter rate that, in turn, is a
key factor in determining its potential feeding rate (Charnov 1976; Nonacs 1991). To increase
opportunities, the ambusher can select specific sites where prey availability is most abundant
and regulate its time schedule based on environmental cues (Putman, Barbour & Clark 2016).
Concomitantly, the ambusher may also attract prey using deception tactics and, hence, further
increase the encounter rate. Such tactics are categorized within the field of mimicry.
The nocturnal behavior of adult females in our study, where tail wriggling was
evident, fits in well with the description of “caudal luring”, described earlier for C. vipera
34
(Heatwole and Davison 1976) and functionally termed “feeding mimicry” (Schuett, Clark &
Kraus 1984). Mimicry involves a degree of similarity or resemblance between organisms, requires responses between the predator and prey, and could be found in various biological systems covering a wide range of biota from plants to animals in a variety of combinations
(Wickler 1965; 1968). Wickler’s description consisted of a tripartite basic system: two different signal transmitters, one being the mimic (S1) and the other being the model (S2), transmitting similar signals to at least one receiver (R). A specific situation is where the model is a small insect commonly preyed upon by a carnivorous vertebrate (R). Another carnivorous vertebrate (S1) presents the mimic to attract its prey (R). This type of deception has been classified as “synergic aggressive mimicry” (Vane-Wright 1976) and, thereafter, was termed “aggressive mimicry” (Glaudas & Alexander 2017; Greene & Campbell 1972;
Jackson & Cross 2013; Reiserer & Schuett 2008). However, as predator-prey interactions are conceptually different from aggressive interactions (Wittenberger 1981), the suggested term
“feeding mimicry” was preferred (Schuett, Clark & Kraus 1984; Pough 1988) to describe the behavioral function in this system.
Typical behavior of feeding mimicry was initially described in fish (e.g. anglerfish;
Wilson 1937; Pietsch & Grobecker 1978) and turtles (e.g. the alligator snapping turtle; Allen and Neill, 1950; Drummond and Gordon, 1979). However, this type of mimicry behavior is most common in snakes that use ambush hunting, mostly viperids, and employs mainly caudal luring (Rabatsky 2008) and, occasionally, lingual luring as a mechanism to deceive potential prey ( Glaudas & Alexander 2017). Other than responses between the snake and its prey, this behavior requires specific modifications at the end of the tail including increased caudal segments for the effective imitation of invertebrate prey (Hampton 2011).
In viperid snakes, many species that use caudal luring when young do not use this technique as adults (Greene 1992). In these species, the tip of the tail is conspicuously
35 colored when young, but this coloring is lost along the ontogenic axis when adulthood is reached. This behavior is attributed to feeding mimicry (Schuett, Clark & Kraus 1984) in which the tip of the tail mimics the typical prey of the receiver, in many cases a lizard
(Hagman, Phillips & Shine 2009; Reiserer 2002; Reiserer & Schuett 2008) or a frog (Glaudas
& Alexander 2017; Reiserer 2002; Schuett, Clark & Kraus 1984). This behaviour is often termed ‘vermiform’ to represent the wriggling of insect larvae (Jackson Cross 2013) used as a prey of lizards. In extreme cases, the deception is so good that the receiver approaches and bites the tip of the tail and that becomes an obligatory trigger for the snake to strike its prey
(Schuett, Clark & Kraus 1984). As adults, these species shift to a different diet (e.g., small mammals) where their luring behavior is not effective and, therefore, not used (Greene
Campbell 1972; Greene 1992; Rabatsky & Farrell 1996). Another extreme case is that of the
Iranian spider-tailed viper, Pseudocerastes urachnoides, where only adults use caudal luring for catching birds as it takes a long time for the deceptive organ to become fully developed.
In this species, the tip of the tail grows to a spider-shape form that lures birds (Fathinia et al.
2015). Only two viperid snakes, Bothrops bilineatus and C. vipera, were reported to use caudal luring along their whole ontogeny; both prey on lizards as young and as adults
(Heatwole and Davison 1976).
Sit-and-wait ambush behavior at night provided nocturnally-active prey mainly for adult females. Adult C. vipera females are slightly larger than males (Sivan et al. 2015), which is a common sexual dimorphism in snakes (Shine 1993; Rivas and Burghardt 2001;
Maritz and Alexander 2011). Also, C. vipera females need more energy for ovoviviparous reproduction (Sivan et al. 2012). However, in this study, body mass and body condition of females that consumed nocturnally-active lizards were similar to females that consumed diurnally-active lizards and, also, were similar to males. Both sexes were mainly sit-and-wait ambushers throughout the night. How then could the higher success in hunting nocturnally
36
active lizard species by females be explained? We surmise that the difference in prey capture between sexes in C. vipera is related to sexual dichromatism. In females, the tips of their tail are black and highly noticeable at night; this pattern is found in females throughout ontogeny but is lacking in males (Marx 1958). Heatwole and Davison (1976) mentioned this sexual dimorphism but concluded “the significance of sexual dimorphism in tail coloration remains obscure in terms of its relation to caudal luring”.
Another sexual dimorphism, not in coloration but in tail morphology is evident in
Sistrurus miliarius barbouri (Bishop et al. 1996), where males have longer tails than females.
Young females and young males use caudal luring at a similar frequency, but females need longer periods to achieve a similar level of foraging success; these differences were attributed to the longer tail in males than females (Rabatsky & Waterman 2005; King et al. 1999), although there might be other reasons for these results. However, conspicuous tail coloration does not necessarily reflect the use of caudal luring; of 66 viperid snakes reported to possess contrasting body and tail colors, only 21 species were reported to employ caudal luring
(Rabatsky 2008). Sexual dichromatism is common among vipers where mainly adult males have more cryptic colors than adult females. This difference is generally attributed to mate selection and sexual behavior (Shine & Madsen 1994). Sexual dimorphism of conspicuous tail coloration in viperid snakes is rare, and has been reported only for C. vipera and Bothrops atrox (Heatwole and Davison 1976; Burger & Smith 1950). However, B. atrox was not reported to use caudal luring, and this dimorphism is absent in adults.
In light of these perspectives, I propose that this sexual dimorphism explains the higher success by females in hunting nocturnally-active lizards. Furthermore, this sexual difference may force males to shift into more diurnal and risky hunting behavior and, thus, differentiate among the quality of individuals, similar to the long and handicap male tail of the peacock (Zahavi and Zahavi 1997). In other words, the lack of blackened tail in males
37 may work as a handicap following Zahavi’s behavioral theory (Zahavi 1975; 1977a, 1977b).
Measurements of hunting times and hunting success could be used to further test this hypothesis.
LIZARDS VS RODENTS AS POTENTIAL PREY
Lizards were the only prey item in this study. This is in agreement with other reports that C. vipera prey exclusively on lizards (Schnurrenberger 1959; Heatwole & Davison 1976;
Subach et al., 2009; Sivan et al 2013). However, rodent pups have been reported to be included in the dietary items of C. vipera (Arbel 1984; Werner 2016) and even composed the major part of its diet in the sands of Northern Algeria (Mermod 1970). I observed rodent activity at the study site, mainly Gerbillus pyramidum and Gerbillus alenbyii. These rodents may be too large as prey when adults, but pups of both species are available in late spring and throughout the summer. While monitoring snake activity, i noticed that adult gerbils of both species exhibited typical antipredator behaviours such as sand kicks, close approaches and jump back in front of C. vipera that lay in an ambush position. This rodent behavior interfered with the ambush strategy of this small snake and the ‘exposed’ viper then usually left its ambush position and moved to another site. Similar rodent anti-predator behaviours were suggested to reduce the likelihood of an attempt to strike by the viperid Crotalus cerastes (Whitford, Freymiller & Clark 2017). It suggests that C. vipera might be a threat to the gerbil and this may be a method to minimize attacks on potential gerbil pups. Although not observed in the present study, it cannot be excluded that in other sandy areas, depending on abundances of rodents and lizards, and population density of the snakes, C. vipera may shift dietary intake towards rodents, as was noted by Mermod (1970).
PREY SIZE AND INTRASPECIFIC SHIFTS IN DIETARY HABITS
38
In viperid snakes, intraspecific differences in dietary habits are mainly attributed to the
ontogenetic axis. In many species, neonates and young prey not only on prey of different size,
but rather on different taxonomic groups. Both neonate and adult C. vipera consumed mainly
diurnally-active lizard species. A major difference was in prey size. Adult C. vipera fed mainly on adult lizards whereas neonates fed exclusively on neonate lizards. Our findings are in agreement with general findings concerning prey size in viperids. Not only do larger snakes hunt larger prey species, but often they refuse to strike at smaller prey items (Shine &
Sun 2003). Consequently, this behavior reduces C. vipera intra-specific competition on resources between neonates and adults, and potentially improves the chances of neonates to overcome and survive the short time period between hatching (ovoviviparity; Sivan et al.
2012; 2015) and hibernation over the winter.
39
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Appendix. Dichotomic key for identifying lizards in C. vipera feces in Wadi Seher based on their claw morphology.
1a. Has a ventral groove ………………..……………………………………...... 2 1b. Does not have a ventral groove …………………C. vipera fang or rear tooth (fig. 4d)
2a. The base of the claw is wider than its distal part…………………………………...... 3 2b. The base of the claw is not wider than its distal part…. Acanthodactylus spp (figs. 4d, A- D, K-M)
3a. The claw have an open ventral groove that start at the bed and covers 2/3 of the length ……Stenodactylus spp. (figs 4d, G-J, O-R) 3b. The claw does not have an open ventral groove that starts at the claw bed and covers less than 2/3 of the claw length…………………………………………………………………….4 4a. At dorsal or ventral view, the claw is wider than in the lateral view…… S. scincus (figs. 4c, A, B, G-I). 4b. At dorsal or ventral view, the claw is narrower than in the lateral view…. S. sepsoides (figs 4c, C-F, J-M).
48