Abstract
Pseudocerastes urarachnoides is a fascinating viper and as yet has been reported only in western Iran. An elaborated arachnid-like caudal structure is a unique feature of this viper, hence gives it the common name “Iranian spider-tailed viper”. During tail wagging, the structure is reminiscent of a moving spider. Tail movements are used for two different purposes in snakes: defense via tail vibration and hunting via both caudal luring and caudal distraction. Caudal luring in snakes is the wriggling or wagging of the posterior part of tail, in the presence of a potential prey, with conspicuous color pattern while the rest of body is cryptically colored. Previous studies have speculated on the role of caudal structure of P. urarachnoides in hunting. Our 2.5-year study has revealed that development of the structure of the caudal lure is commenced after birth and is linearly correlated to snout-vent length. The caudal lure attracts some species of birds. Caudal luring behavior is carried out both in the presence and absence of birds. The findings are reported for the first time and confirmed by direct observation of undisturbed individuals in the field.
Introduction
Snakes are capable of communication through visual, olfactory, tactile or acoustical signals. A snake’s body can be divided into different parts including: head, neck, trunk and tail. Each part may serve as a signaling device for intra- and interspecific communication (Carpenter, 1977). Squamate tails are used for different purposes including defense by autotomy, defense by rattling/vibrating, aggression and feeding (Foster and Martin, 2008). Rattles, in the subfamily Crotalinae, for example, are specialized structures evolved for defense purposes by vibrating tail tip and making a rattling sound. Defensive function of the tail has also been reported in the family Colubridae (Mullin, 1999). Despite defensive function, snakes also use their tails for caudal luring and to distract prey and/or predators (Mullin, 1999). Caudal luring in snakes is the wriggling or wagging of the posterior part of the tail, in the presence of a potential prey. Tail tip, in caudal luring snakes, usually has a conspicuous color pattern while the rest of body is cryptically colored (Freitas and Silva, 2011). Prey luring behavior has been reported for many snake families including Boidae (Murphy et al., 1978; Radcliffe et al., 1980), Colubridae (Sazima and Puorto, 1993; Leal and Thomas, 1994; Tiebout, 1997), Elapidae (Carpenter et al., 1978; Chiszar et al., 1990) and Viperidae (Kauffeld, 1943; Neill, 1948; Allen, 1949; Wharton, 1960; Henderson, 1970; Greene and Campbell, 1972; Heatwole and Davison, 1976; Jackson and Martin, 1980; Schuett, 1984; Carpenter and Gillingham, 1990; Sazima, 1991; Rabatsky and Farrell, 1996; Daltry et al., 1998; Parellada and Santos, 2002; Whitaker and Captain, 2004; Rabatsky, 2008; Freitas and Silva, 2011).
Apparently caudal luring is a plesiomorphic trait for the viperids and has independently evolved at least twice in squamate reptiles (i.e. in snakes and one gekkonid) (Rabatsky, 2008). It seems that caudal luring behavior is used more frequently in viperids than other snakes (Farrell et al., 2011). So far, 7.5% of the viperids have been documented to use caudal luring (Rabatsky, 2008). In caudal distraction, the movements of tail parallel that of caudal luring and defensive tail vibration. In caudal distraction both the tail – head distance and speed of tail movements is greater than in caudal luring (Mullin, 1999). The adaptive significance of this movement is the distraction of the snake’s prey (Mullin, 1999) or predator (Rabatsky, 2008) from the head of the snake toward its tail.
Postnatal development of caudal lure in the Iranian spider-tailed viper, Pseudocerastes urarachnoides. SVL of the specimens: a = 198, b = 265, c = 305, d = 320, e = 360, f = 450, g = 500, h = 590, i = 620, j = 690, k = 765 and l = 875 mm. This figure is published in colour in the online version.
Citation: Amphibia-Reptilia 36, 3 (2015) ; 10.1163/15685381-00002997
Pseudocerastes urarachnoides Bostanchi, Anderson, Kami and Papenfuss, 2006, is a fascinating viper from western Iran. The Iranian spider-tailed viper was first collected (holotype, FMNH 170292) in Ilam province during the Second Street Expedition to Iran in 1968. The second specimen (paratype) was collected in western Kermanshah province, between Guilan-e-Gharb and Qasr-e-Shirin (Bostanchi et al., 2006). A unique feature of this viper is an elaborate caudal structure which gives it the common name “Iranian spider-tailed viper”. While tail wagging, the structure is reminiscent of a spider on the move (Fathinia, 2014). Until 2009 the only information about this viper was it occurrence in western Iran along with incomplete data on its morphology (Bostanchi et al., 2006). Fathinia et al. (2009) conducted a survey to reveal some aspects of this viper’s biology including habitat description, distribution, and the usage of caudal structure. Despite a profound morphological difference between P. urarachnoides and its congeners (P. fieldi and P. persicus), a recent molecular study has shown that the Iranian spider-tailed viper belongs to the genus Pseudocerastes and is a closer relative to P. persicus than to P. fieldi (Fathinia et al., 2014). The elaborate tail structure in the Iranian spider-tailed viper, Pseudocerastes urarachnoides, has resulted in speculation on the function of the caudal structure (Bostanchi et al., 2006; Fathinia et al., 2009). We videotaped undisturbed individuals in the field to gain insight into the different aspects of P. urarchnoides such as the percentage of time in ambush, the frequency of tail luring and to see if tail luring differs in the presence or absence of a bird, to describe the dynamic of the caudal luring, to identify prey items, to reveal allometric growth of the caudal structure and finally to see if different strategies are used during feeding.
Material and methods
We captured twelve individuals of the Iranian spider-tailed viper, Pseudocerastes urarachnoides for morphological measurements. The study site was located in Bina and Bijar No-hunting area (33°39′N, 45°58′E), Ilam province, western Iran. The survey was carried out during 2.5 years, from May 2011 to October 2013. During activity seasons (i.e. spring, summer and autumn), we surveyed the study area one week per month on average. To trace the development of the caudal structure we measured snout-vent length (SVL) by a tape measure and tail length (TL), length of knob-like structure (LKS), and length of last caudal appendage in the close proximity of its knoblike structure (LLCA) using a digital caliper to the nearest 0.01 mm. To record tail movements, prey attraction by caudal luring and hunting behavior, we used digital Handy-Cams (models Sony xr520, Sony xr550, and Sony ex3). Due to small number of cameras and time-limitation in using the cameras, only three out of the twelve specimens were filmed. To determine the presence or absence of avian prey during recording, the corresponding author hid in a camouflaged tent, around 15 meters away, where he could carefully watch the field of study. Of course the presence of a researcher in the home range of the Iranian spider-tailed viper, both during setting up and removing the cameras, might have negative impacts on its behavior and cause the halting of tail luring. To avoid such negative impacts in the statistics of caudal luring behavior we determined the time interval between first (after setting up the cameras) and last (before removing the cameras) movements of tail luring. The raw data of recorded footages of tail luring was retrieved in software Corel VideoStudio Pro X4, to reveal the rate of tail luring. We retrieved 44 minutes of tail luring from three individual vipers, in a total 155 minutes of filming. We calculated the frequency of each movement of tail luring from beginning to end, as well as time interval taken to perform each of the tail movements. We defined a cycle of tail luring as a lateral movement of distal half of tail which starts from a certain point (called starting point) to the opposite point (end of trajectory) and then backs again to the starting point. To calculate the frequency per time unit, we divided frequency (Hz) by time (second). We used Shapiro-Wilk for testing data normality to choose between a parametric or nonparametric test for analyzing TW (tail wagging) data in the two different conditions (i.e. presence versus absence of avian prey). SPSS 16 was used to analyze the raw data of caudal luring and to see if there is any significant difference in the rate of tail luring in the presence and/or absence of avian prey. To reveal and measure allometric relationships between LKS and LLCA as predicted variables and body size (SVL) as predictor variable, a linear function (Y = aX + b) was computed in SPSS. Prior to computing the allometric equation, the values of predictor and predicted variables were log-transformed.
Results
Postnatal development of caudal lure
Analyzing 12 individuals of the Iranian spider-tailed viper with different SVLs revealed that the caudal lure appears postnatally. At the SVL of approximately 20 cm the tail has a simple structure like that of other viperines. A gradual change starts in the tail tip as a swelling in the last pair of dorsal and ventral scales. Thereafter, an elongation in the lateral, dorsolateral and dorsal scales of the last half of the tail occurs. Along with the development of a knoblike structure the elongation of scales is accompanied by a dorsal to ventral rolling of them, which finally leads to an elaborate caudal structure (fig. 1).
A diagram showing the frequency of tail luring in Pseudocerastes urarachnoides in the absence and presence of avian prey. Those five peaks with frequencies higher than 0.3 and black solid asterisks above, indicating caudal luring when avian preys present. This figure is published in colour in the online version.
Citation: Amphibia-Reptilia 36, 3 (2015) ; 10.1163/15685381-00002997
Both log LKS and log LLCA were strongly correlated with log SVL. Slope of regression line for LLCA (1.7) was greater than that for LKS (1.16). Correlations, r, for the regression are 0.978 and 0.979 for LKS and LLCA, respectively. The values of r2 (0.956 for LKS and 0.958 for LLCA) indicates that around 96% of the variation in predicted variables is explained by the regression line. Both equations have high estimation accuracy (high r2).
The developmental rate of the last caudal appendage parallels that of the knob-like structure, but crisscrosses it at around SVL of 50 cm; LLCA starting from a smaller size than LKS, starts to grow a bit faster around 4 mm, surpasses LKS at the size of 8 mm, and tend to stabilize around 14 mm, while LKS stabilizes on a smaller size around 12 mm.
Prey attraction and dynamics of caudal luring
The time each of the three vipers has spent tail luring was counted and analyzed. The Iranian spider-tailed viper spent 28.5% of the total time in ambush sites (i.e. 2646 out of 9283 seconds) caudal luring. A total of 121 cases of tail luring out of 155 minutes of filming were recorded for the three vipers that caudal lured. Birds were clearly present in only five out of 121 cases. The senior author did not observe prey in the remaining 116 cases of tail luring. The mean frequency of tail luring in the absence of birds was 0.093 ± 0.0041 (Mean ± SD) Hz (min and max was 0.009 and 0.285 Hz, respectively) and with a bird it was 0.381 ± 0.0289 Hz (min and max were 0.307 and 0.471 Hz, respectively) (fig. 2). TW data had non-normal distribution (P < 0.0001). Results of the Wilcoxon Signed-Ranks test showed a significant difference between tail luring in the absence and presence of avian prey (P < 0.05).
The evaluation of tail luring revealed that the posterior half of the tail is engaged in caudal luring. A wave is commenced as lateral movement (left-right or right-left) of distal half of tail. The Distal half shows two continuous movement phases. (a) Preliminary movement phase during which the proximal part of distal portion moves around in a lateral (left to right or right to left) axis with angles of around 45° at most; and (b) following the movement, a complementary movement starts during which the distal half of distal portion, including caudal appendages (or presumptive legs of spider) and knob-like structure (the presumptive abdomen of spider), moves further around in the lateral axis and reaches the end of trajectory. While caudal luring, ‘legs of spider’ take a more elevated position than in the resting phase, making an angle of around 90°, more or less, to the longitudinal axis of tail. A brief video of this tail movement can be seen on YouTube (courtesy of Behzad Fathinia; search for Pseudocerastes urarachnoides).
Prey items and feeding behavior
A sub-adult specimen of spider-tailed viper, with SVL of around 30 cm, regurgitated an adult Persian gecko, Hemidactylus persicus. Video sequences (from April 2011 to June 2013) revealed six successful predatory attempts on different bird species by the spider-tailed viper. These prey items included one Isabelline Shrike, Lanius isabellinus and five warblers, Acrocephalus sp. However, only one case of the predations recorded the attraction of birds toward caudal luring (fig. 3), whereas, the other five remaining footages were recorded from the moment when the birds were in the mouth of the Iranian spider-tailed viper, because the predation had already been initiated before arrival of researcher at the habitat and setting up the cameras.
A complete scene of predation on birds by the Iranian spider-tailed viper, Pseudocerastes urarachnoides. (a) A motionless Iranian spider-tailed viper while caudal luring, (b) attacking the tail by bird, (c-d) fleeing from the vipers fang, (e) returning toward the caudal lure, (f) pecking the tail, (g) striking of this viper, (h) biting and envenoming the prey on the head, (i) fluttering for escape, (j) simultaneously swallowing and pulling in the dead bird. This figure is published in colour in the online version.
Citation: Amphibia-Reptilia 36, 3 (2015) ; 10.1163/15685381-00002997
A brief description of the complete predation event includes the Iranian spider-tailed viper calmly wagging its tail from motionless coil (fig. 3a), suddenly a warbler lands on the head of this viper, attacks toward the “spider” on the move, i.e. the caudal lure (b), the Iranian spider-tailed viper strikes the bird (c), but the bird flees from its fangs (d) and moves out of imaging frame, then the bird comes back to attack the spider (e), capture it (f), and this time the Iranian spider-tailed viper attacks the bird, mouth open (g), bites the bird on the head (h), the bird flutteringly tries to escape from the mouth of this viper (i), but after around 90 seconds it dies, and around seven minutes later the Iranian spider-tailed viper pulls the bird into its hole while swallowing it (j). From the first appearance of the bird in the recording frame to capture by the Iranian spider-tailed viper took 1.14 seconds (i.e. 33 frames) and it took around 0.2 seconds from pecking caudal lure by the bird to capture by the Iranian spider-tailed viper. The predation video is published as online supplementary material at http://dx.doi.org/10.6084/m9.figshare.1454446.
Various strategies in feeding on birds were observed. In one case a viper released an envenomated dead bird and then displayed SICS behavior (Strike Induced Chemosensory Search), seeking the prey while tongue flicking. In four cases the Iranian spider-tailed vipers held onto the prey and after the death of the prey trying to swallow it over the ground (i.e. on perches or in crevices at the rock or limestone walls) with jaw movements looking for proper position (head of the bird), while not allowing the prey to fall out from the mouth. In another case a viper released an envenomated dead prey on the edge of its ambush site, not falling to the ground from the height, and then seeking for its head while tongue flicking.
In one of the footages an Iranian spider-tailed viper, in the presence of a nearby adult western-rock nuthatch (Sitta neumayer), a year-round resident, was rapidly wagging its tail. The western-rock nuthatch, in searching for food, approached the Iranian spider-tailed viper cautiously while keeping a distance of around one meter. The bird carefully oriented towards the moving spider (i.e. caudal lure) but did not approach it. This viper stopped luring but the bird cautiously searched, while keeping a safe distance. The bird jumped on a perch one to two meters away from the Iranian spider-tailed viper, and suddenly the luring action was started once more. The luring movements lasted only for four cycles and stopped once more. The bird was jumping from one twig to another while monitoring the space around. Finally the bird flew off the area. The sequence lasted for around seven minutes.
We noticed that the caudal lure was prone to damage. In one case, an adult female that had recently lost its knob-like structure, was observed with some blood clots on its tail tip. This injury may be the result of a deceived prey successfully pecking the lure.
Discussion
Caudal luring behavior by the Iranian spider-tailed viper, P. urarachnoides, was documented for the first time through this study. Some cryptically ‘sit and wait’ snakes take advantage of the caudal luring behavior. They wait in ambush sites while invoking predatory behavior of potential prey, via tail wriggling, to approach them closely enough to be caught (Simon et al., 1999; Farrell et al., 2011). Observation on caudal luring in P. urarachnoides confirms the speculations of previous authors, who based their conjectures mainly on the presence of partially digested bird remains associated with the paratype specimens (Bostanchi et al., 2006; Fathinia et al., 2009). Caudal luring has been defined as a behavior triggered by the presence of a potential prey (Freitas and Silva, 2011), but the definition is not completely true for the Iranian spider-tailed viper as we observed and recorded caudal luring behavior both in the absence and presence of potential prey and only the intensity of the behavior differs in the absence and presence cases. Some researchers have emphasized the contrast in color between tail tip and the rest of body (Neill, 1960; Heatwole and Davison, 1976; Rabatsky, 2008) which may suggest an important role for the tail color in the rate of predatory success. Farrell et al. (2011) have indicated that tail color has no significant role in the predatory success of juveniles Sistrurus miliaris. The tail of P. urarachnoides is not contrastingly colored, and this may be indicative of the greater contribution of tail luring pattern than tail color in successful predation. The study has revealed that the Iranian spider-tailed viper spends around one third of total time tail wagging in ambush sites. The presence of a bird potential prey is a triggering agent; the frequency of tail wagging behavior gets more intense and increases by about four times when the birds were observed nearby.
Warblers and butcher birds (shrikes) are migratory passerines which travel each year from Africa to Eurasia for breeding in the spring and back again in autumn for wintering (Newton, 2008). In determining preyed items no year-round resident birds were identified. Predation on migratory birds may show more efficiency of the caudal structure in deceiving migratory birds than resident ones. This may indicate that resident birds, due to the long period of their presence in the habitat and long-term encounter with this viper, have learned to avoid the lure and to identify the vipers, while the migratory ones have not. Several species of vipers including Bothrops insularis (Wüster et al., 2005; Andrade et al., 2010) and Gloydius shedaoensis (Shine and Li-Xin, 2002) are also highly dependent on consuming migratory birds.
The Persian false-horned viper, Pseudocerastes persicus, preys upon lizards, rodents, (Latifi, 2000; Phelps, 2010) and arthropods (Khan, 2002), and also feeds on migratory birds during spring and autumn (Mallow et al., 2003). Predation upon birds has also been reported for the Field’s horned viper, Pseudocerastes fieldi (Disi, 2002). Although, feeding upon birds is proven for P. urarachnoides through this study, the contribution of birds in its diet, in comparison to its congeners, remains uncertain. Regarding the elaborate caudal lure in P. urarachnoides, we assume that, especially in adulthood, birds comprise a considerable part of its diet. But the claim needs to be proved. Regarding postnatal development of tail structure, its role in attracting birds and hence in subsistence of the Iranian spider-tailed viper, and lacking of caudal structure and of conspicuousness in color of tail tip in juveniles, some questions may arise: Is there any dietary shift along with gradual progress of caudal lure in the Iranian spider-tailed viper? Whether juveniles have a sit and wait or an active foraging strategy? And what is the composition of juveniles’ diet? Obviously, leg of sun-spiders (Solifugae) and spiders is longer than the length of the abdomen and arranged in a perpendicular position to the proximal-distal axis of the body. We presume that a longer length of the last caudal appendage than the knob-like structure in adulthood, accompanied by an almost perpendicular position of the appendages to the longitudinal axis of tail during luring, may make the wagging movements appear more similar to the prey items (i.e. spiders or sun spiders) used by insect-eating birds and thereby encourage the birds to attack the wagging tail. The consumption of Hemidactylus gecko indicates that this viper is an opportunistic predator, feeding on reptiles as well as birds, or even may be indicative of dietary shift during ontogeny of the Iranian spider-tailed viper.
Tail tip mutilation or missing is an indication of predation pressure in herpetological studies (Arnold, 1994) and has been reported in ambush snakes showing tail wriggling behavior to attract prey (Andrade et al., 2010). For example, Bothrops insularis, an endemic species to the Queimada Grande Island, southeastern Brazil (Marques et al., 2002; Martins et al., 2002), feeds mainly on two species of migratory passerine birds, Elaenia chilensis and Turdus flavipes, in adulthood (Marques et al., 2012) and on frogs, lizards and centipedes in childhood (Marques et al., 2002; Martins et al., 2002). Andrade et al. (2010) have shown the mutilation of tail tip in both B. insularis (20.9% of studied specimens) and B. jararaca (7.3%). Although the caudal structure of P. urarachnoides is an efficient means for deceiving avian prey, the elaborated structure, especially swelling of tail tip, is exposed to damage which may be caused by the beaks of insect-eating birds. The rate of such injuries of the caudal lure and its subsequent impact on the success of prey deception and finally in survival of the Iranian spider-tailed viper is not clear.
Acknowledgements
We wish to thank Mahmood Mansouri and Mehdi Noormohamadi for their great efforts in recording many of the scenes. We wish to thank Steven C. Anderson, University of Pacific, Stockton, California, and Marco Mangiacotti, Museo Civico di Storia Naturale, Milano, Italy for their kindness in editing and improving the paper. We also appreciate the authorities of Razi University and Department of Ilam Environment for their support during the study. Permission for capturing and studying the species was issued by DOE of Iran (91/50451). A part of this work was supported by funding from Ilam Center for Broadcasting, Ilam province, Iran to produce the documentary film “Life in Cold Veins”, which shows the behavior described here far more dramatically than words can describe.
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Footnotes
Associate Editor: Sylvain Ursenbacher.
