The spitting behavior of two species of spitting cobras

Spitting cobras defend themselves by spitting their venom in the face of a harasser. Although it is common belief that spitting cobras direct their venom at the eyes of an aggressor, this has never been investigated. Here, we show that the spitting act of cobras (Naja nigricollis and N. pallida) can readily be triggered by a moving human face or by a moving real size photo of a human face. In contrast, a stationary human face (real or photo) or a moving or stationary human hand does not trigger the spitting act. If threatened, spitting cobras aim their venom, ejected either in two distinct jets (N. pallida) or in a fine spray (N. nigricollis), either between the eyes or at one eye. In both cobra species investigated, the width and height of the area hit by the venom was independent of eye distance (test range 5.5 cm and 11 cm). During the spitting act the cobras performed fast undulating head movements that lead to a larger distribution of their venom. This behavior increases the probability that at least one eye of the aggressor is hit. Electronic Supplementary Material Supplementary material is available for this article at     

Potential targets aimed at by spitting cobras when deterring predators from attacking

When threatened, spitting cobras eject venom towards the face of an aggressor. To uncover the relevant cues used by cobras for face recognition we determined how often artificial targets equipped with or without eyes elicited spitting behavior. In addition, we measured whether and how target shape and size influenced the spitting behavior of cobras. Results show that oval- and round-shaped targets were most effective, while triangles with the same surface area as oval ‘face like’ targets hardly elicited spitting. The likelihood of spitting depended on neither the presence, the spatial arrangement (horizontal or vertical) nor the surface texture (shiny or matt) of glass eyes. Most likely, cobras do not specifically aim at the eyes of an offender but at the center of the body part closest to them. As this is usually the face of an animal, this strategy will result in at least one eye of the offender being hit most of the time.     

The ghost of a recent invasion in the reduced feeding rates of spitting cobras during the dry season in a rainforest region of tropical Africa?

Two species of cobras (Naja melanoleuca and Naja nigricollis) are known to occur in south eastern Nigeria, where much of the pristine rainforest surface has been felled in the last thirty years, and where the actual landscape is generally constituted by a mosaic of farmlands, plantations, suburban areas, with a few remnant forest fragments. In this region, Naja nigricollis is currently extending its range, especially by exploiting recently deforested areas. Based on the known general distribution range of this species and on the available literature data, it appears that Naja nigricollis has been colonizing the forested region of south eastern Nigeria, starting from the relatively arid savannas of central Nigeria, where this species aestivates during the driest months. In the forest region, however, snakes do not need to aestivate during the dry season. Nevertheless, whereas Naja melanoleuca has a foraging activity extended all-the-year round, Naja nigricollis reduces feeding rates during the dry months, although it does not suspend above-ground activity in these months. I suggest that rainforest spitting cobras suspend feeding during the dry months because their behaviour is just a ‘ghost’ of their recent past, when they were ‘normal’ spitting cobras of dry savana regions, which were thus constrained to aestivate during the dry season as it is the rule in this species in central and northern Nigeria. The ‘gost-of-the-past hypothesis’ seems to fit well with the ‘invading’ presence of Naja nigricollis in Nigerian areas where they were reported as rare or, even, absent, up to a few decades ago. Other hypotheses are discussed, and rejected.     

Cover-seeking behavior in red spitting cobras (Naja mossambica pallida): Effects of tactile cues and darkness

Eleven red spitting cobras, Naja mossambica pallida, used clear Plexiglas hiding boxes as frequently as they used dark ones in a successive discrimination paradigm (experiment 1), which indicated that thigmotaxic cues can satisfy the cover-seeking needs of the snakes. In simultaneous discrimination tests, however, dark places were always preferred by the snakes (experiments II, III). Therefore, although thigmotaxic cues are sufficient, these plus darkness constitute a more favorable alternative for N m pallida. The husbandry advantages associated with clear hiding boxes, together with their sufficiency for the snakes, argue strongly for their use in many captive environments.     

Geographical differentiation and cryptic diversity in the monocled cobra,Naja kaouthia (Elapidae), from Thailand

South‐East Asia has an exceptionally high diversity of snakes, with more than 250 snake species currently recorded from Thailand. This diversity likely reflects the diverse range of geographical and climatic conditions under which they live, but the evolutionary history and population genetics of many snake species in South‐East Asia have been little investigated in comparison with morphological studies. Here, we investigated genetic variation in the monocled cobra, Naja kaouthia, Lesson, 1831, across its distribution range in Thailand using mitochondrial DNA (cytochrome b, control region) for ~100 individuals and the nuclear DNA gene (C‐mos) for a small subset. Using population genetic and phylogenetic methods, we show high levels of genetic variation between regional populations of this non‐spitting cobra, including the north‐eastern, north‐central and southern regions, in addition to a population on Pha‐ngan Island, 150 km offshore from the southern peninsula. Moreover, inclusion of the north‐eastern population renders N. kaouthia paraphyletic in relation to other regional Naja species. The north‐eastern population is therefore probably specifically distinct. Given that these cobras are otherwise undifferentiated based on colour and general appearance to the “typical” cobra type of this region, they would represent a cryptic species. As has been shown in other animal groups from Thailand, it is likely that the geographical characteristics and/or tectonic alteration of these regions have facilitated high levels of population divergence of N. kaouthia in this region. Our study highlights the need for dense sampling of snake populations to reveal their systematics, plan conservation and facilitate anti‐snake venom development.     

The phylogeny of cobras inferred from mitochondrial DNA sequences: evolution of venom spitting and the phylogeography of the African spitting cobras (Serpentes: Elapidae: Naja nigricollis complex)

We use phylogenetic analysis of 1333 bp of mitochondrial DNA sequence to investigate the phylogeny and historical biogeography of the cobra-like elapid snakes, with special reference to the evolution of spitting and the phylogeography of the African spitting cobras, a radiation widespread in open vegetational formations throughout sub-Saharan Africa. Our results suggest that spitting adaptations appear to have evolved three times in cobras, but alternative scenarios cannot be rejected. The Asiatic Naja are monophyletic and originate from a single colonization of Asia from Africa. The radiation of the African spitting Naja appears to date back to the early Miocene and many speciation events in the group predate the Pliocene expansion of grasslands and the radiation of large grazing mammals in Africa. The cladogenic events in this complex appear to have been triggered by both ecological changes and tectonic events associated with the formation and expansion of the African Rift Valley. Taxonomically, our data confirm the inclusion of Boulengerina and Paranaja within Naja, and reveal a clade of African rainforest cobras including N. melanoleuca, Paranaja multifasciata and Boulengerina that constitutes the sister clade of the African open-formation non-spitting cobras. Naja nigricollis is polyphyletic, and we therefore recognize N. nigricincta as a separate species, more closely related to N. ashei and N. mossambica than to N. nigricollis.     

Localization of the site of effect of a wasp's venom in the cockroach escape circuitry

The parasitic wasp Ampulex compressa stings a cockroach Periplaneta americana in the neck, toward the head ganglia (the brain and subesophageal ganglion). In the present study, our aim was to identify the head ganglion that is the target of the venom and the mechanisms by which the venom blocks the thoracic portion of the escape neuronal circuitry. Because the escape responses elicited by a wind stimulus in brainless and sham-operated animals were similar, we propose that the venom effect is on the subesophageal ganglion. Apparently, the subesophageal ganglion modulates the thoracic portion of the escape circuit. Recordings of thoracic interneuron responses to the input from the abdominal giant interneurons showed that the thoracic interneurons receive synaptic drive from these interneurons in control and in stung animals. Unlike normal cockroaches, which use both fast and slow motoneurons for producing rapid escape movements, stung animals activate only the slow motoneuron. However, we show that in stung animals, the fast motoneuron still can be recruited with bath application of pilocarpine, a muscarinic agonist. These results indicate that the descending control from the subesophageal ganglion is presumably exerted on the premotor thoracic interneurons to motoneurons connection of the thoracic escape circuitry. Accepted: 19 December 1998     

Stimulus control of predatory behaviour in red spitting cobras (Naja mossambica pallida) and prairie rattlesnakes (Crotalus v. viridis)

Two experiments examined the responses of red spitting cobras (Naja mossambica pallida) to stimulus properties of rodent prey. In experiment 1 cobras exhibited elevated rates of tongue flicking (RTF) and trail-following behaviour after striking mice and after 15-s presentations of visual-chemical-thermal cues arising from mice held just out of striking range. Disturbance with a clean snake hook did not produce similar effects. In experiment 2 these cobras were compared with prairie rattlesnakes (Crotalus v. viridis). All snakes were exposed to five stimulus conditions in their home cages: (1) 3 s of disturbance (D) with a clean snake hook; (2) 15 s of D; (3) 3 s inspection of a live mouse held out of striking range (NS); (4) 15 s of NS; and (5) a presentation of a live mouse inside striking range (S). The snakes always struck in the latter condition, usually within 3 s. Rattlesnakes exhibited elevated RTF only after S, whereas cobras did so after 15 s of both NS and S. The performance of rattlesnakes was consistent with the assumption that these animals are ambushers; that of cobras was consistent with the assumption that these animals are active hunters which will chase and catch visually detected prey.     

Regulation and Non-Toxicity of the Spit from the Pale Spitting Spider Scytodes Pallida (Araneae: Scytodidae)

The pale spitting spider Scytodes pallida (Aranae: Scytodidae) has a unique habit of spitting a glue‐like and possibly toxic substance at its prey to render them immobile prior to envenomation. Quantitative behavioural studies involving the spit, a first for S. pallida, demonstrate that the spider regulates its spit expenditure when offered prey of variable sizes and struggling intensities. This behaviour interestingly mirrors the regulation of venom expenditure according to prey sizes and difficulties exhibited in other non‐spitting spiders. The spit, however, did not appear to have any toxic effects on different prey types exposed to the spit, opposing the long‐standing belief that the spit from scytodids can poison prey.     

Tests of a linear model of visual-vestibular interaction using the technique of parameter estimation

The goal of this study was to test whether a superposition model of smooth-pursuit and vestibulo-ocular reflex (VOR) eye movements could account for the stability of gaze that subjects show as they view a stationary target, during head rotations at frequencies that correspond to natural movements. Horizontal smooth-pursuit and the VOR were tested using sinusoidal stimuli with frequencies in the range 1.0–3.5 Hz. During head rotation, subjects viewed a stationary target either directly or through an optical device that required eye movements to be approximately twice the amplitude of head movements in order to maintain foveal vision of the target. The gain of compensatory eye movements during viewing through the optical device was generally greater than during direct viewing or during attempted fixation of the remembered target location in darkness. This suggests that visual factors influence the response, even at high frequencies of head rotation. During viewing through the optical device, the gain of compensatory eye movements declined as a function of the frequency of head rotation (P < 0.001) but, at any particular frequency, there was no correlation with peak head velocity (P > 0.23), peak head acceleration (P > 0.22) or retinal slip speed (P > 0.22). The optimal values of parameters of smooth-pursuit and VOR components of a simple superposition model were estimated in the frequency domain, using the measured responses during head rotation, as each subject viewed the stationary target through the optical device. We then compared the model's prediction of smooth-pursuit gain and phase, at each frequency, with values obtained experimentally. Each subject's pursuit showed lower gain and greater phase lag than the model predicted. Smooth-pursuit performance did not improve significantly if the moving target was a 10 deg × 10 deg Amsler grid, or if sinusoidal oscillation of the target was superimposed on ramp motion. Further, subjects were still able to modulate the gain of compensatory eye movements during pseudo-random head perturbations, making improved predictor performance during visual-vestibular interactions unlikely. We conclude that the increase in gain of eye movements that compensate for head rotations when subjects view, rather than imagine, a stationary target cannot be adequately explained by superposition of VOR and smooth-pursuit signals. Instead, vision may affect VOR performance by determining the context of the behavior. Received: 16 June 1997 / Accepted: 5 December 1997     

The Visual Orientation Strategies of Mantis religiosa and Empusa fasciata Reflect Differences in the Structure of Their Visual Surroundings

In the present study, peering behaviour, which is used to measure distance by the image motion caused by head movement, is examined in two types of mantid. Mantis religiosa inhabits a region of dense grass consisting of uniform, generally uniformly aligned, and closely spaced elements and executes slow, simple peering movements. In contrast, Empusa fasciata climbs about in open regions of shrubs and bushes which consist of irregular, variably aligned and variably spaced elements and it executes comparatively quick, complex peering movements. Hence, it seems that in these two species of mantid, the same orientation mechanism has been adapted to the unique structures of their visual surroundings. Apparently M. religiosa uses motion parallax and E. fasciata uses a combination of motion parallax and forward and backward movements (image expansion/contraction over time) to detect object distances.     

Prey size selection and distance estimation in foraging adult dragonflies

To determine whether perching dragonflies visually assess the distance to potential prey items, we presented artificial prey, glass beads suspended from fine wires, to perching dragonflies in the field. We videotaped the responses of freely foraging dragonflies (Libellula luctuosa and Sympetrum vicinum—Odonata, suborder Anisoptera) to beads ranging from 0.5 mm to 8 mm in diameter, recording whether or not the dragonflies took off after the beads, and if so, at what distance. Our results indicated that dragonflies were highly selective for bead size. Furthermore, the smaller Sympetrum preferred beads of smaller size and the larger Libellula preferred larger beads. Each species rejected beads as large or larger than their heads, even when the beads subtended the same visual angles as the smaller, attractive beads. Since bead size cannot be determined without reference to distance, we conclude that dragonflies are able to estimate the distance to potential prey items. The range over which they estimate distance is about 1 m for the larger Libellula and 70 cm for the smaller Sympetrum. The mechanism of distance estimation is unknown, but it probably includes both stereopsis and the motion parallax produced by head movements.     

The embryonic development of the Egyptian cobra Naja h. haje (Squamata: Serpentes: Elapidae)

The Egyptian cobra, Naja h. haje, is the largest of the African cobras and is a member of a successful and medically important species complex found throughout Africa, north and south of the Sahara, as well as across the Arabian Peninsula to Oman. Although its phylogenetic position and venom characteristics have been well studied, its development has not. Here, we present a normal staging table for N. h. haje, based on external features. Comparison with firstly the Asian monocled cobra, Naja kaouthia, and then with the small number of other oviparous snake species, allowed us to examine whether differences between two species in the same genus were of the same type and magnitude as those between unrelated genera. In fact, at least with respect to external features, we found a similar level of disparity. N. h. haje embryos lagged behind those of N. kaouthia in body and head scale development, size in ovo and hatchling length, despite having a slightly shorter incubation period and a somewhat larger adult size. Some of these differences may have been the result of differing incubation temperatures. Nonetheless, there does appear to be a broadly conserved pattern of in ovo development in at least macrostomatan snakes.     

Effects of damping head movement and facial expression in dyadic conversation using real–time facial expression tracking and synthesized avatars

When people speak with one another, they tend to adapt their head movements and facial expressions in response to each others'' head movements and facial expressions. We present an experiment in which confederates'' head movements and facial expressions were motion tracked during videoconference conversations, an avatar face was reconstructed in real time, and naive participants spoke with the avatar face. No naive participant guessed that the computer generated face was not video. Confederates'' facial expressions, vocal inflections and head movements were attenuated at 1 min intervals in a fully crossed experimental design. Attenuated head movements led to increased head nods and lateral head turns, and attenuated facial expressions led to increased head nodding in both naive participants and confederates. Together, these results are consistent with a hypothesis that the dynamics of head movements in dyadicconversation include a shared equilibrium. Although both conversational partners were blind to the manipulation, when apparent head movement of one conversant was attenuated, both partners responded by increasing the velocity of their head movements.     

Responses of collicular fixation neurons to gaze shift perturbations in head-unrestrained monkey reveal gaze feedback control

A prominent hypothesis in motor control is that endpoint errors are minimized because motor commands are updated in real time via internal feedback loops. We investigated in monkey whether orienting saccadic gaze shifts made in the dark with coordinated eye-head movements are controlled by feedback. We recorded from superior colliculus fixation neurons (SCFNs) that fired tonically during fixation and were silent during gaze shifts. When we briefly (相似文献   

Prey pursuit and interception in dragonflies

Perching dragonflies (Libellulidae; Odonata) are sit-and-wait predators, which take off and pursue small flying insects. To investigate their prey pursuit strategy, we videotaped 36 prey-capture flights of male dragonflies, Erythemis simplicicollis and Leucorrhinia intacta, for frame-by-frame analysis. We found that dragonflies fly directly toward the point of prey interception by steering to minimize the movement of the prey's image on the retina. This behavior could be guided by target-selective descending interneurons which show directionally selective visual responses to small-object movement. We investigated how dragonflies discriminate distance of potential prey. We found a peak in angular velocity of the prey shortly before take-off which might cue the dragonfly to nearby flying targets. Parallax information from head movements was not required for successful prey pursuit. Accepted: 11 November 1999     

Saccadic head and thorax movements in freely walking blowflies

Visual information processing is adapted to the statistics of natural visual stimuli, and these statistics depend to a large extent on the movements of an animal itself. To investigate such movements in freely walking blowflies, we measured the orientation and position of their head and thorax, with high spatial and temporal accuracy. Experiments were performed on Calliphora vicina, Lucilia cuprina and L. caesar. We found that thorax and head orientation of walking flies is typically different from the direction of walking, with differences of 45° common. During walking, the head and the thorax turn abruptly, with a frequency of 5–10 Hz and angular velocities in the order of 1,000°/s. These saccades are stereotyped: head and thorax start simultaneously, with the head turning faster, and finishing its turn before the thorax. The changes in position during walking are saccade-like as well, occurring synchronously, but on average slightly after the orientation saccades. Between orientation saccades the angular velocities are low and the head is held more stable than the thorax. We argue that the strategy of turning by saccades improves the performance of the visual system of blowflies.     

Cobra Venom Cytotoxin Free of Phospholipase A2 and Its Effect on Model Membranes and T Leukemia Cells

Membrane-active toxins from snake venom have been used previously to study protein-lipid interactions and to probe the physical and biochemical states of biomembranes. To extend these studies, we have isolated from Naja naja kaowthia (cobra) venom a cytotoxin free of detectable phospholipase A₂ (PLA₂). The amino acid composition, pI (10.2), and net charge of the cytotoxin compares well with membrane-active toxins isolated from venoms of other cobras. The cytotoxin, shown by a spin label method, associates with PLA₂ in buffers at pH values between 7.0 and 5.0, but not at pH 4.0. It is suggested that cytotoxin and PLA₂ (pI close to 4.8) associate electrostatically in the native venom. The effect of the cytotoxin on model phospholipid membranes was studied by EPR of spin probes in oriented lipid multilayers and ¹H-NMR of sonicated liposomes. The cytotoxin did not significantly affect the packing of lipids in pure phosphatidylcholine (PC) membranes and in PC membranes containing 10 mol% phosphatidic acid (PA) or cardiolipin (CL). However, the cytotoxin induced an increase in membrane permeability and formation of nonbilayer structures in PC membranes containing 40 mol% of PA or CL. The purified cytotoxin was cytocidal to Jurkat cells, but had little effect on normal human lymphocytes. However, both Jurkat cells and normal lymphocytes were killed equivalently when treated with 10⁻⁹ m PLA₂ and 10⁻⁵ m cytotoxin in combination. From its effect on model membranes and Jurkat cells, it is suggested that purified cytotoxin preferentially targets and disrupts membranes that are rich in acidic phospholipids on the extracellular side of the plasma membrane. Received: 20 March 1996/Revised: 25 September 1996     

Functional morphology of the sting apparatus of the spider wasp Cryptocheilus versicolor (Scopoli, 1763) (Hymenoptera: Pompilidae)

The females of the spider wasps (Hymenoptera: Pompilidae) hunt spiders to provision their larvae. The genital structures of pompilid females are modified in a sting that is used for paralyzing the prey (spiders) and defense. The skeleto‐muscular structure of the sting apparatus of a typical representative of the family (Cryptocheilus versicolor) is examined. The shape of sclerites, their relative positions and articulations are described. Some morphological adaptations are described for the first time. The wide anal arc of the tergum IX provides a stiff support for the muscles that move the valvulae. The resilin structures in the areas of articulation support the work of muscles and in some cases replace them. The 1st valvulae form a venom duct along their entire length, which provides the delivery of the venom to a specific point. An unpaired flap in the venom duct provides a dose of venom in the sting. This mechanism probably enhances the speed and accuracy of the wasp's sting movements. Functions of muscles and interactions of the structures of the sting apparatus of C. versicolor are discussed.     

Snake venomics of African spitting cobras: toxin composition and assessment of congeneric cross-reactivity of the pan-African EchiTAb-Plus-ICP antivenom by antivenomics and neutralization approaches

Venomic analysis of the venoms of Naja nigricollis, N. katiensis, N. nubiae, N. mossambica, and N. pallida revealed similar compositional trends. The high content of cytotoxins and PLA(2)s may account for the extensive tissue necrosis characteristic of the envenomings by these species. The high abundance of a type I α-neurotoxin in N. nubiae may be responsible for the high lethal toxicity of this venom (in rodents). The ability of EchiTAb-Plus-ICP antivenom to immunodeplete and neutralize the venoms of African spitting cobras was assessed by antivenomics and neutralization tests. It partially immunodepleted 3FTx and PLA(2)s and completely immunodepleted SVMPs and CRISPs in all venoms. The antivenom neutralized the dermonecrotic and PLA(2) activities of all African Naja venoms, whereas lethality was eliminated in the venoms of N. nigricollis, N. mossambica, and N. pallida but not in those of N. nubiae and N. katiensis. The lack of neutralization of lethality of N. nubiae venom may be of medical relevance only in relatively populous areas of the Saharan region. The impaired activity of EchiTAb-Plus-ICP against N. katiensis may not represent a major concern. This species is sympatric with N. nigricollis in many regions of Africa, although very few bites have been attributed to it.