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1 Role of ribs in antipredatory behaviour

Course of Herpethology | Matteo Lattuada

1. Abstract

This essay is focused on the description of antipredatory behaviours displayed by some species of amphibians and reptiles. Concerning the amphibians, I described species of Salamandridae family, namely the genera Echinotriton, Tylototriton and Pleurodeles with a species in example for each genus: Echinotriton andersoni, Tylototriton verrucosus and Pleurodeles waltl. These animals have very particular skills, in fact, they can pierce their body with their own ribs to wound and repel predators. Anurans, instead, have the ribs fused with the spine, thus, the cannot show any defensive technique based on these bones. Afterwards, I reported the technique of hooding in the Naje genus, underlining more in detail the morphological events that take place during the hooding progress. Similarly, I also delineated the most important information to know how the lung inflation works in lizards, taking as example the chuckwalla, Sauromalus obesus. Furthermore, I briefly mentioned the evolution of buccal pumping. In conclusion, comparing the use of ribs as antipredatory behaviour in reptiles and amphibians, I found out that within many genera of reptiles, the ribs are important structures to base their defence on. While in amphibians exists just one family which is able to exploit the ribs in case of attack.

2. Introduction.

This essay focuses on some morphological and physiological peculiarities used by different reptiles and amphibians to defend themselves when attacked or to defend their burrows. Most amphibians lack conspicuous weapons. However, some Southeast Asian voiceless frogs have evolved different forms of protection like tusks, spines and larger head (Emlen, 2008) and ribs (Heiss et al., 2011; Nowak & Brodie, 1978; Brodie et al., 1984). The amphibians described in this paper belong to three species: Pleurodeles waltl, Echinotriton andersoni and Tylototriton verrucosus. Their genera are members of a monophyletic clade and are considered sister groups (Weisrock, 2006). While the formers are able to protrude their ribs, the latter does not show this peculiarity (Heiss et al, 2009). Dinosaurs have developed a broad range of odd structures which is thought were needed for self defence or for fighting which have been gradually lost in later descendants, when many of these

structures become larger and more spectacular, functioning mainly as ornaments with a visual purpose (Emlen, 2008). Many extant reptiles lost the complex body parts present in dinosaurs, but they show other fascinating skills. For example, many lizards employ conspicuous buccal movements in addition to respiration, which are used even to wedge himself in crevice or to augment the animal volume in response to nuisance (Deban et al., 1994). Instead, cobras species (Naia Haje and Naja kaouthia) display the hooding, that is a spectacular and efficient method to avoid predation.

3. Description of the techniques.


Ribs function in Salamandridae.

The Salamandridae have the greatest diversity of antipredatory behaviour of all salamanders (Brodie et al., 1984). Here, I describe the newts belonging to the genera Pleurodeles, Echinotriton and Tylototriton which have been included in the same clade thanks to the support of genetic studies (Weisrock et al, 2006). It seems that the Asiatic genera Tylototriton and Echinototriton derive from the European ancestor Pleurodeles (Veith, 2004). These three genera developed an antipredation technique which entails the anterior rotation of the ribs. However, only Pleurodeles and Echinototriton achieve an extreme conformation, piercing their skin (Heiss, 2009). Instead, Tylototriton erects his ribs pressing on his warts to facilitate the toxic excretions, without puncture the skin (Brodie et al., 1984).

Pleurodeles waltl. Pleurodeles waltl is a species of salamander native to Spain and Morocco (Weisrock et al., 2006). This species, as the Echinotriton genus, can pierce itself skin with its ribs. These animals can rely on their granular glands that produce different bioactive substances. When the ribs exit from the body, they collect the toxic compounds on the skin. Thus, when a predator bites them on the ribs, it will be stung and it will flee away (Nowak and Brodie, 1978). P. waltl has 8-10 warts on each of his side that signals the toxicity of the animal. Furthermore, when harassed, he adopts his defensive position directing the head of the ribs outwards, perpendicularly to the major body axis (Heiss et al, 2011; Nowak and Brodie, 1978). P. waltl shows his more spectacular position only when he is attacked from the side or when it is picked up (Nowak and Brodie, 1978). In these occasions, the body is lifted in an arch shape with the tail on the ground, occasionally coiled. The head is flexed downward and the forelimbs flexed

locating all the animal mass on the digits (Nowak and Brodie, 1978). In the relaxed condition the ribs lay oriented backward, but in case of stimulation, the vertebral column is held straight and the ribs are rotated forward by the dorsalis trunci musculature until the achievement of a maximum angle of 92° relative to the longitudinal axis of the corresponding vertebra (Heiss et al, 2011). Finally, the muscles of the rectus abdominis are used to retract the ribs after posturing (Nowak and Brodie, 1978). The ribs have particular characteristics that increase the effectiveness of their defence. They are longer than in other salamander species (Nowak and Brodie, 1978) and embedded in muscle fibres that coordinate their rotation. They possess a particular costovertebral joint that constrains deflexion and enable the rotation forward (Heiss et al, 2011). Furthermore, a thick layer of loose connective tissue is present where the skin will be pierced, likely to facilitate repairing the hole caused by ribs penetration. Additionally, while the three quarter of the ribs proximal to the spine are filled of fat tissue, the tip is made of bony tissue coated by a periostium. This robust structure helps the ribs to penetrate in the flesh of the predator (Heiss et al, 2011). Finally, P. waltl is armoured with two different granular glands producing bioactive compounds, like alkaloids, which are harmful for any predator and secreted in the external skin when the animal is disturbed (Heiss et al, 2009). This unique defensive behaviour, where sharp ribs are dip in toxic glands, seems to be really effective. Experimental evidences showed that the hedgehog Hemiechinus auritus (which feed on salamanders) avoided individuals of P. waltl after the first bite of one of them (Nowak and Brodie, 1978).

Asiatic newts. As stated above, the two genera Tylototriton and Echinotriton are close relatives of Pleurodeles. In fact, they also exploit their ribs like weapons against predators. Tylototriton resemble the Pleurodeles for some characteristics like the diverse postures to face different type of attacks, but he is unable to pierce his skin with the ribs (Heiss, 2011; Brodie et al., 1984). This seems linked to the fact that the centre of warts in Tylototriton contains granular glands, which is not the case for related skin-piercing genera (Nowak and Brodie, 1978). Echinotriton andersoni, similarly to P. waltl, lacks of granular glands in the midpoint of the warts. In fact, he can use the ribs and even the tips of the epipleural process, which are both placed right under the warts centre, to plunge the enemies Also in E. andersoni, the distal third of ribs and the epipleural process are void of muscles, but immersed in connective tissue to ease

the piercing. In particular, the ribs from the third to the ninth of each side are more elongated and sharp. If on the one hand, the mechanism of ribs rotation in E. andersoni looks like the one in P. waltl where the ribs are brought forward until an angle of about 90° with the vertebral column axis (Brodie et al., 1984). On the other hand, the postures of the two species differ. E. andersoni does not protect the snout, but he elevates tail and head, showing the bright colours in palms of the forelimbs and under the tail. Furthermore, E. andersoni presents vertebrates with anteriorlycurved tips projecting laterally from the quadrate bone which lies next to glandular glands. The presence of these tips seems to exclude the predation by snakes because the reptiles cannot swallow the newts (Brodie et al., 1984).

Additional features of amphibians. It is important to underline the role of toxins excrete by amphibians like amines, peptides, proteins, steroids, and both water-soluble and lipid-soluble alkaloids, which increase the efficiency of their antipredatory behaviour. The alkaloids are mainly retrieved from arthropods included in the diet (Daly et al., 2005; Daly 1995). Some of these compounds, like tetrodotoxins, found in many species of newts (Yotsu et al. 1990; Brodie et al.,1974), are powerful neurotoxins mortal for human beings (Hwang & Noguchi, 2007). However, the compounds synthesized in the granular glands of the genera described in this essay do not cause death in humans. Nonetheless, the quantity extracted from 1.2 granular gland of P. waltl is sufficient to kill a mouse (Nowak and Brodie, 1978). The piercing of the skin in environments with high concentration of potential infective microbiological fauna may likely provoke some diseases. Thus, some amphibians specimens have developed a resistant immune system which is helped by skin peptides to withstand infections (Schadich, 2009). It seems to be likely also for P. waltl, because they do not show any symptom of infection on the punctures (Heiss et al., 2011) and E. andersoni.


Ribs function in reptiles.

The use of ribs to support defensive inflation in reptiles has been reported in at least 19 species of lizards, 25 species of snakes and two species of crocodilians (Deban et al., 1994). Besides this behaviour, the ribs are crucial in one of the most fascinating visual display in nature: the hooding

of cobras, well described for Naja haje and Naja kaouthia in the paper of Young and Kardong, published in 2010.

The cobras

Ribs morphology Cobras need particular morphological structure to exhibit the hooding. Hence, the proximal surface of the rib and diapophysis from the region of the hood have more rounded, simpler articular surfaces than the ribs and parapophyses from the mid-body, to allow a wider bony movement (Young and Kerdong, 2010). Here, the ligaments are constituted by abundant elastic connective tissue. In the neck the span of the ribs gradually increases from the first to the 7th-8th rib and then decreases again. The length of the ribs increase rapidly in the firsts four ribs and then follow steady decrease until the 20th rib of the neck that measure the same size of the rest of the body (Young and Kerdong, 2010).

Hooding During the hooding, the ribs rotate obtaining a cranial protraction and a dorsal elevation, with the neck ribs displaying the higher angular magnitude with the vertebral column. The ribs expansion begins cranially and spread caudally. The displacement can be stopped, with the hood held partially erected for more than 10 minutes. However, also the complete hood can be maintained for long time depending on the stimulus provided and on individual attitude. The hooding per se is fully displayed in 80 ms thanks to the coordination of several muscles. There are four main phases setting up the hooding (Young and Kerdong, 2010): 1. The hooding starts with the activation of the muscles costovertebrocostalis, intercostalis externus and tubercolocostalis, which concur to displace the neck and the posterior ribs. 2. The levator costae, which has specialized origins and insertions, is the primary effector for the hood erection, it is activated shortly before the onset of ribs displacement and it is active throughout the maintenance of the hooding. Also the supracostalis lateralis superior is slightly employed for the lifting of the neck, but its main function is the protraction of the firsts ribs. 3. Costocutaneous superior, costocutaneous inferior and obliquos abdomines internus connect the skin with the ribs, keeping the skin taut when the animal is erected. 4. The relaxation occurs when the iliocostalis and the oblique internus parsdorsalis are activated and work against the supracostalis lateralis superior levator costae which are deactivated. At

the same time, the ligament that span the caudoventral surface of the costovertebral joint recoils, allowing costocutaneous inferior, costocutaneous superior and tubercolocostalis to facilitate the ribs displacement.

The Chuckwalla (Sauromalus obesus). Nearly all the amphibians and reptiles living in crevices escape into their shelter when a predator approaches. However, some of them, like the chuckwalla (Sauromalus obesus), inflate their body to press themselves against the wall of the fissure to avoid to be extracted (Witt & Caldwell, 2009). The chuckwalla is able to exert into its lungs a volume of air four times the normal quantity inspired during breath thanks to buccal pumping (Deban et al., 1994). Buccal pumping is a technique used by many reptiles in addition to aspiratory thoracic breathing. It seems to be employed to enlarge the olfactory sense and during courtship, as well as defensive behaviour (Al-Ghamdi et al., 2001). Normally, when reptiles are increasing their size with the buccal pumping, the nares are sealed to avoid leak that will prevent the achievement of high pressure. Hence, the normal respiration does not take place (Deban et al., 1994). Nonetheless, in the end of the ninety’s, it has been discovered that in the genus Varanus, the buccal pump can assist the lung ventilation during locomotion (Owerkowicz et al., 1999). The inflation of chuckwallas has four main phases resumed below (Deban et al., 1994): 1. The tongue is moved rostrodorsally, sealing the nares, in order to increase the pressure in the buccal cavity until it exceeds the one in the lungs. 2. The glottis opens letting the air passing from the buccal cavity to the lungs thanks to difference in the pressure potential. The air continues to flow until the pressure in the lungs peaks and it cannot increase further. 3. When the external stimulus disappeared, the buccal cavity expands and the pressure drops permitting the air flowing from lungs to the gular cavity. Thus, the pressure in the buccal cavity increase over the atmospheric one, so the nares open and the air can be released. 4. The buccal cavity continues to expand until the pressure inside equalize the pressure in the air. At this point the physiological conditions are reinstated and the animal can breathe normally. The role of ribs in this displacement is fundamental for the success of the defence. In fact, when chuckwalla inflates in crevices, the buccal pumping forces the ribs beyond the maximum excursion that the hypoxial musculature would produce during aspiration. In addition, the gular pumping fills the lungs up to four times the normal aspiration volume and the ribs are extended wider than during normal respiration. Furthermore, while in the common breathing the ribs

tension must be maintained actively by the intercoastal musculature, the inflation with buccal pumping does not stress the muscles and the air in the lungs is directed in all the directions towards the crevice wall, fixing the animal in the fissure. Indeed, only the glottal musculature and some pulses are required to maintain the position (Deban et al., 1994). Interestingly, also some anurans evolved the buccal pumping as antipredatory behaviour even if they do not have ribs (Hodl & Amezquita, 2001; Wang et. al, 1999). In fact, reptiles and amphibians derived this technique from a common ancestor (Deban et al., 1994). Therefore, buccal pumping originated from the acquatic pump that is used by bony fish to irrigate their gills. After the divergence of tetrapods in the Devonian (Benton, 1990), the evolution of aspiration pump relegated the buccal pump just as an accessory role in respiration in many lizards. Just later, some species like Sauromalus obesus and Uromastix aegyptius specialized the function of buccal pumping to inflate their lungs when disturbed (Deban et al.,1994).

4. Conclusion.

As described above,in amphibians, the family Salamandridae is the only one which use ribs like efficient weapons to repel predators, particularly when used together with toxins (Heiss et. al., 2009; Nowak and Brodie, 1978; Heiss et al., 2011; Brodie et al., 1984). Reptiles, instead, have at least two defensive behaviour where the ribs play crucial role. The most common is the swelling due to lung inflation that is displayed in different genera and it is used either to awe the enemies or to embed themselves in a crevice (Deban et al.; 1994).the most fascinating is found in true cobras (Naje) and some closely related elapids (e.g. Ophiophagus), beside them, hoods are also known from a variety of other snakes (e.g. Hydrodynastes). Thus, it could be a synapomorphy in Xenodontine snakes. A sort of hooding less impressive and specialized is also present in Acanthophis species (Young & Kerdong, 2010). However, this visual display occurs in few genera, therefore it can be stated that hooding is a peculiar trait evolved just in narrow range of snakes with a suitable set of ribs. Finally, while some salamanders posture and even use their ribs actively to drive back enemies, other amphibians do not have antipredatory behaviour based on ribs movements. On the contrary, in reptiles, the ribs have a broader range of utilization and they are particularly important to display impressive conformation to avoid predation.

5. References.

Al-ghamdi, M. S., & Jones, J. F. (2001). Evidence of a functional role in lung inflation for the buccal in pump in the agamid lizard uromastyx aegyptius microlepis. The journal of experimental biology 204 , 521–531. Benton, M. J. (1990). Phylogeny of the major tetrapod groups: morphological data and divergence dates. Journal of molecular evolution , 409-424. Brodie, E. D., Hensel, J. L., & Johnson, J. A. (1974). Toxicity of the urodele amphibians taricha, notophthalmus, cynops and paramesotriton (salamandridae). Copeia vol. 1974, no. 2 , 506-511. Brodie, E. D., Nussbaum, R. A., & Digiovanni, M. ( 1984). Antipredator adaptations of asian salamanders (salamandridae). Herpetologica, 40(1) , 56-68. Daly, J. W., Spande, T. F., & Garraffo, H. M. ( 2005). Alkaloids from amphibian skin: a tabulation of over eight-hundred compounds. J. Nat. Prod., 68 , 1556-1575. Daly, J. W. (1995). The chemistry of poisons in amphibian skin. Proc. Natl. Acad. Sci. USA, 15 Deban, S. M., O’reilly, J. C., & Theimer, T. (1994). Mechanism of defensive inflation in the chukwalla, sauromalus obesus. The journal of experimental zoology 270 , 451-459. Emlen, D. J. (2008). The evolution of animal weapons. Reviews in advance , 387-425. Heiss, E., Natchev, N., Rabanser, A., Weisgram, J., & Hilgers, H. (2009). Three types of cutaneous glands in the skin of the salamandrid pleurodeles waltl. A histological and ultrastructural study. Journal of morphology 270 , 892-902. Heiss, E., Natchev, N., Salaberger, D., Gumpenberger, M., Rabanser, A., & Weisgram, J. (2011). Hurt yourself to hurt your enemy: new insights on the function of the bizarre antipredator mechanism in the salamandrid pleurodeles waltl. Journal of zoology , 156-163. Hödl, W., & Amezquita, A. (2001). Visual signaling in anuran amphibians. In: , (m.j. Ryan, ed.). Anuran communication , 121-141. Hwang, D., & Noguchi, T. (2007). Tetrodotoxin poisoning. Advances in food and nutrition research , 141–236. Nowak, T. R., & Brodie, E. D. (1978). Rib penetration and associated antipredator adaptations in the salamander pleurodeles waltl (salamandridae). Copeia , 424-429. Owerkowicz, T., farmer, C. G., Hicks, J. W., & Brainerd, e. L. (1999). Contribution of gular pumping to lung ventilation in monitor lizards. Science 284 , 1661-1665.

Schadich, E. (2009). Skin peptide activities against opportunistic bacterial pathogens of the african clawed frog (xenopus laevis) and three litoria frogs. Journal of herpetology, 43(2) , 173-183. Veith, M., mayer, C., Samraoui, B., Barroso, D. D., & Bogaerts, s. (2004). From europe to africa and vice versa: evidence for multiple intercontinental dispersal in ribbed salamanders (genus pleurodeles). Journal of biogeography (j. Biogeogr.) 31 , 159–171. Vitt, l. J., & Caldwell, j. (2009). Herpethology. An introductionary biology of amphibians and reptiles. San diego: elsevier. Wang, T., Hedrick, M. S., Ihmied, Y. M., & taylor, e. W. (1999). Control and interaction of the cardiovascular and respiratory systems in anuran amphibians. Comparative biochemistry and physiology part a 124 , 393–406. Weisrock, D. W., papenfuss, T. J., macey, J. R., & Litvinchuk, S. N. (2006). A molecular assessment of phylogenetic relationships and lineage accumulation rates within the family salamandridae (amphibia, caudata). Molecular phylogenetics and evolution 41 , 368–383. Yotsu, M., Iorizzi, M., & Yasumoto, T. (1990). Distribution of tetrodotoxin, 6-epltetrodotoxin, and 11-deoxytetrodotoxin in newts. Toxicon vol. 28 , 238-241. Young, B. A., & Kardong, K. V. (2010). The functional morphology of hooding in cobras. The journal of experimental biology 213 , 1521-1528.