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Morphological and Ecological Correlates of Bite Force in the Rockdwelling Lizards Ouroborus Cataphractus And

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Morphological and Ecological Correlates of Bite Force in the Rockdwelling Lizards Ouroborus Cataphractus And bs_bs_banner Biological Journal of the Linnean Society, 2014, 111, 823–833. With 4 figures Under pressure: morphological and ecological correlates of bite force in the rock-dwelling lizards Ouroborus cataphractus and Karusasaurus polyzonus (Squamata: Cordylidae) Downloaded from https://academic.oup.com/biolinnean/article/111/4/823/2415797 by guest on 28 September 2021 CHRIS BROECKHOVEN* and P. LE FRAS N. MOUTON Department of Botany & Zoology, Stellenbosch University, Private Bag X1, Matieland 7602, Stellenbosch, South Africa Received 31 October 2013; revised 2 December 2013; accepted for publication 2 December 2013 Rock-dwelling lizards are hypothesized to be highly constrained in the evolution of head morphology and, consequently, bite force. Because the ability to generate a high bite force might be advantageous for a species’ dietary ecology, morphological changes in head configuration that allow individuals to maintain or improve their bite force under the constraint of crevice-dwelling behaviour are to be expected. The present study addressed this issue by examining head morphology, bite force, and a number of dietary traits in the rock-dwelling cordylid lizards Ouroborus cataphractus and Karusasaurus polyzonus. The results obtained show that O. cataphractus has a larger head and higher bite force than K. polyzonus. In K. polyzonus, head width, lower jaw length, and jaw closing-in lever are the best predictors of bite force, whereas head height is the main determinant of bite force in O. cataphractus. Although the observed difference in bite force between the species does not appear to be related to dietary patterns or prey handling, the prey spectrum available for intake was greater in O. cataphractus compared to K. polyzonus. We discuss the influence of interspecific differences in anti-predator morphology on head morphology and bite force in these rock-dwelling species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 823–833. ADDITIONAL KEYWORDS: ecomorphology – feeding – head morphology – prey handling – prey hardness – sexual dimorphism. INTRODUCTION to external selective pressures imposed by environ- mental factors (Vitt et al., 1997; Vanhooydonck & Van The cranial system of vertebrates is a complex inte- Damme, 1999; Herrel, De Grauw & Lemos-Espinal, grated system and is responsible for an array of 2001a; Lappin, Hamilton & Sullivan, 2006; Kohlsdorf functions and behaviours, including feeding, drinking, et al., 2008; Revell et al., 2007; Vanhooydonck et al., chemoreception, display, and defence (Bels, Goosse & 2010; Barros, Herrel & Kohlsdorf, 2011). Kardong, 1993; Schwenk, 1995, 2000). For an organ- In lizards, the evolution of head morphology has ism, it is often not possible to optimize these functions been hypothesized to be influenced by habitat use. To simultaneously because the selective pressures on the illustrate, head size appears to be constrained in different components of the cranial system are con- burrowing skinks (Barros et al., 2011) because selec- flicting in many cases, leading to functional trade-offs tion for a large head will increase burrowing time (e.g. fish: Westneat, 1994; turtles: Herrel, O’Reilly & and, consequently, predation risk (Vanhooydonck Richmond, 2002; birds: Herrel et al., 2009). Moreover, et al., 2011). In lacertid lizards, a large head appears not only is the cranial system affected by conflicts to negatively affect climbing performance by shifting between internal components, but also it is subjected the lizard’s centre of mass away from the substrate (Vanhooydonck & Van Damme, 1999; Vanhooydonck, Herrel & Van Damme, 2007). Similarly, the use of *Corresponding author. E-mail: [email protected] crevices by rock-dwelling species appears to constrain © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 823–833 823 824 C. BROECKHOVEN and P. LE F. N. MOUTON head morphology (Herrel et al., 2001a; Lappin et al., 2006; Revell et al., 2007; Kaliontzopoulou et al., 2012; but see Kohlsdorf et al., 2008) because a tall head prohibits individuals from using narrow crevices, thereby increasing the risk of becoming extracted by predators (Cooper, Van Wyk & Mouton, 1999; Cooper et al., 2000). The constraints of crevice-dwelling behaviour on head morphology might impair bite performance because changes in form, size, and relative position of cranial and muscular elements greatly affect bite force Downloaded from https://academic.oup.com/biolinnean/article/111/4/823/2415797 by guest on 28 September 2021 (Herrel et al., 1999, 2001a, b, 2006; Lappin & Husak, 2005; Herrel, McBrayer & Larson, 2007; Brecko et al., 2008). A reduction in bite force, in turn, can have major consequences for a species’ diet because it may limit the proportion of hard prey available for intake (Herrel et al., 1999, 2001b; Aguirre et al., 2003; Marshall et al., Figure 1. Photographs of the heads of Ouroborus 2012) or affect prey selection through prolonged han- cataphractus (left) and Karusasaurus polyzonus (right) in dling duration for harder and/or larger prey (Andrews dorsal (top) and lateral (bottom) views to illustrate differ- & Bertram, 1997; Verwaijen, Van Damme & Herrel, ences in head shape. 2002). A study by Kaliontzopoulou et al. (2012) showed that, although microhabitat divergence between two lizard species is reflected in their head morphology, crevice and the terrestrial predation pressure associ- a rock-dwelling lifestyle does not constrain bite force ated with these foraging excursions (Mouton, 2011). or diet. These findings suggest that the presence of Despite the use of a clumped food source (i.e. ter- morphological changes in head configuration serves to mites) away from the communal crevice, competition maintain bite force, thereby allowing rock-dwelling between group-members appears to remain high species to utilize similar dietary resources as terres- (Mouton, Geertsema & Visagie, 2000; Shuttleworth trial species. et al., 2008). The concurrence of a short activity peak The present study aimed to provide more insight with high arthropod abundance at the end of the into the relationships between head morphology, rainy season appears to counteract the negative bite force, and several aspects of dietary ecology effects of group-living behaviour, thereby allowing using two rock-dwelling cordylid lizards, Ourobo- individuals to survive the dry season (Flemming & rus cataphractus (Boie, 1828) and Karusasaurus Mouton, 2002; Shuttleworth, Mouton & Van Niekerk, polyzonus (Smith 1838) (Fig. 1), as study organisms. 2013). By contrast, K. polyzonus is a strictly solitary, The two species are closely related (Stanley et al., moderately armoured species that does not display 2011) and are considered as strict rock-dwelling sit- tail-biting behaviour. Karusasaurus polyzonus has an and-wait foragers (Mouton & Van Wyk, 1997). They overall generalistic diet (De Waal, 1978; Branch & co-occur throughout their distribution range (Branch, Bauer, 1995; Branch, 1998) and is active throughout 1998) and are often observed sharing the same rock the year (Visagie, 2001). Furthermore, although crevices (Effenberger & Mouton, 2007). Ouroborus males in the group-living O. cataphractus display ter- cataphractus and K. polyzonus, however, strongly ritorial polygyny (Effenberger & Mouton, 2007), only differ in several aspects of their behaviour and mor- low levels of intraspecific aggression have been phology. Ouroborus cataphractus is a group-living, observed in K. polyzonus (P. le F. N. Mouton, pers. heavily armoured species that will grip its tail observ.). between the jaws when threatened by predators The first aim of the present study was to investi- and roll up into an impenetrable ball, with the gate which morphometric variables contribute to bite spiny tail and legs protecting the soft underparts force in the two rock-dwelling species. We predicted (Mouton, Flemming & Kanga, 1999; Losos et al., that (1) head width and length of the jaw closing 2002; Mouton, 2011). During the long dry season, in-lever are better predictors of bite force than head individuals sporadically visit the foraging ports of the height, which is constrained by crevice dwelling- southern harvester termite, Microhodotermes viator behaviour, and that (2) the effect is more pronounced (Shuttleworth, Mouton & Van Wyk, 2008). It has been in O. cataphractus because a higher bite force is hypothesized that the heavy armour and tail-biting presumably beneficial for tail-biting behaviour. The behaviour in O. cataphractus are direct consequences second aim was to examine whether bite force influ- of exploiting termites away from the safety of the ences aspects of the dietary ecology of the two species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 823–833 CREVICE-DWELLING BEHAVIOUR AND BITE FORCE 825 We predicted that (3) an increase in bite force Collection of the University of Stellenbosch. All speci- increases the number of hard-bodied prey items than mens came from the same geographical area and can be consumed and reduces the time needed to stomach contents belonged to individuals caught at process a given prey item. different times of the year to rule out any possibility of seasonal variation in diet. All remains were iden- tified to order level, with the exception of larvae (i.e. MATERIAL AND METHODS Lepidoptera, Diptera, Coleoptera), which were treated MORPHOLOGY AND BITE FORCE separately as a result of their sedentary nature, A sample
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