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No Trade-Off Between Biting and Suction Feeding Performance In 27 The Journal of Experimental Biology 210, 27-36 Published by The Company of Biologists 2007 doi:10.1242/jeb.02619 No trade-off between biting and suction feeding performance in clariid catfishes Sam Van Wassenbergh1,*, Anthony Herrel1, Dominique Adriaens2 and Peter Aerts1,3 1Department of Biology, Universiteit Antwerpen, Universiteitsplein 1, B-2610 Antwerpen, Belgium, 2Evolutionary Morphology of Vertebrates, Ghent University, K.L. Ledeganckstraat 35, B-9000 Gent, Belgium and 3Department of Movement and Sports Sciences, Ghent University, Watersportlaan 2, B-9000 Gent, Belgium *Author for correspondence (e-mail: [email protected]) Accepted 26 October 2006 Summary It is generally assumed that biting performance trades without compromising suction performance. The amount off with suction performance in fish because both feeding of buccal expansion in the ventral direction is types may place conflicting demands on the cranial approximately equal for all species. Consequently, the musculo-skeletal system. However, the functional system generating expansion through ventral rotation of consequences of morphological adaptations enhancing the lower jaw, hyoid and pectoral girdle is apparently not biting on the mechanics and performance of suction constrained (mechanically or architectonically) by the feeding in fish remain obscure. In this study, suction hypertrophy of the jaw adductors. As the effect of a feeding performance was compared between three clariid reduced magnitude of lateral expansion (suspensorium catfish species differing considerably in their biting abduction) on suction performance in Clariidae appears to capacity, by measuring the velocity of a standardized prey be negligible (for example in Gymnallabes typus), these being sucked into the buccal cavity using high-speed data demonstrate the dominant role of ventral expansion cineradiography. In addition, buccal volume changes for producing suction in these fish. during prey capture were quantified by ellipse modelling. As all species were able to accelerate the prey to similar peak velocities, our results demonstrate the possibility for Key words: prey capture, X-ray video, kinematics, catfish, buccal catfishes to increase bite performance considerably volume. Introduction system of fishes (Liem, 1980). It has to cope with capturing, Evolution towards optimal performance is prevented processing and transporting prey, breathing water or air, whenever two ecologically relevant functions require opposing participating in sensory perceptions, providing protection for biomechanical or physiological adaptations (Stearns, 1992). the major sense organs and brains, and serving as a streamlined Such evolutionary trade-offs are often observed in case certain bow in locomotion. Logically, each of these functions calls for components of the musculo-skeletal system have to participate specific, structural and dynamical requirements to the animal’s in different functions: a certain change in one aspect of the cranial system. As a result, the morphological diversity in a system increases the performance of a given function, but at certain trait exhibited in taxa will be evolutionary constrained the same time may reduce the organism’s efficiency in due to the disparate functional demands on this trait. This was performing an other, morphologically coupled function (e.g. demonstrated recently in the oral jaw system of Labrid fishes Vanhooydonck and Van Damme, 2001; Van Damme et al., (Alfaro et al., 2005). 2002; Pasi and Carrier, 2003; Schondube and Del Rio, 2003). Different functional aspects can also be distinguished within Identifying such conflicts in the performance of ecologically the process of prey capture: prey can either be caught by relevant functions is basic to our understanding of the suction feeding (generating a flow of water that drags the prey evolutionary processes associated with species radiations. towards and into the mouth) and/or by biting (e.g. scraping Furthermore, analyses of the constraints on the compatibility algae or picking molluscs off the substrate with the oral jaws). of functions may provide insight into the ecological potential It is hypothesised that biting a prey or sucking it directly into (potential niche width) of animals (Barel, 1983). the mouth are two functionally conflicting ways of getting food One of the most striking examples of a complex and into the buccal cavity (Barel, 1983; Bouton et al., 1999; Sibbing integrated system that has to fulfil a large number of crucial and Nagelkerke, 2001). It is therefore assumed that suction biological functions is probably the cranial musculo-skeletal feeding and biting can be combined only to a certain extent, THE JOURNAL OF EXPERIMENTAL BIOLOGY 28 S. Van Wassenbergh and others and at certain costs. This hypothesis appears to be supported species, this group of fishes provides a unique opportunity to by the observation that specialized biters usually possess other test the proposed trade-off between suction and biting anatomical, functional, dietary and behavioural features that performance in a number of evolutionary lineages. It also distinguish them from species that rely primarily upon suction allows us to examine the biomechanical consequences of the feeding to capture prey (Alfaro et al., 2001). morphological variation associated with increasing bite However, many fish species still seem to combine biting and performance on the kinematics of buccal cavity expansion. suction seemingly efficiently (Turingan and Wainwright, 1993; Bouton et al., 1998; Van Wassenbergh et al., 2004; Janovetz, 2005), and to our knowledge, no experimental study has yet Materials and methods directly demonstrated the proposed inverse relationship Species, morphology, phylogeny and bite performance between biting and suction performance (see Bouton et al., According to a recent molecular phylogenetic study (Jansen 1998). Consequently, the underlying biomechanical basis et al., 2006), species with eel-like bodies, hypertrophied jaw responsible for the proposed conflicting demands on the oral adductors and a narrow skull roof have arisen at least four times jaw apparatus (for biting) and the buccal expansion apparatus independently within the Clariidae. Each time, a sister group (for suction feeding) remains to be demonstrated. relation with a non-specialized Clarias-like ancestor is In this paper, suction performance is quantified and observed. In this study, we focus on two lineages from which compared between species of air-breathing catfish (Clariidae) three clariid species were selected (Fig.·2): Clarias gariepinus that differ in bite performance. In this group of fishes, (Burchell 1822), Gymnallabes typus (Günther 1867) and hypertrophy of the jaw adductors (Fig.·1) is a derived feature Channallabes apus (Günther 1873). that has evolved at least four times independently (Jansen et The neurocranium of C. gariepinus forms a broad, closed al., 2006) and is associated with a drastic increase in maximal roof that partly covers the relatively small jaw adductor bite force (Herrel et al., 2002) and a larger proportion of hard muscles (Cabuy et al., 1999). Its overall cranial morphology prey (mainly coleopterans) in the diet (Huysentruyt et al., resembles that of Heteropneustes fossilis, which can be 2004). Nevertheless, our observations have shown that even the considered as a sister species of Clariidae (Agnese and Teugels, species with the most extreme jaw adductor hypertrophy still 2005; Diogo, 2005; Jansen et al., 2006). Biomechanical apply considerable buccal expansion before impacting the jaws modelling has shown that the maximal bite forces that can be onto the prey, and manage to drag relatively large prey into the exerted by C. gariepinus are considerably less than species with mouth by suction. Furthermore, as Clariidae appear to generate jaw adductor hypertrophy (Herrel et al., 2002) (Fig.·2). Yet, C. suction predominantly by expanding their buccal cavity in the gariepinus has a broad diet, which not only includes relatively ventral direction (Van Wassenbergh et al., 2004), the fact that soft prey such as insect nymphs, fish and shrimps, but also the jaw adductors are bulging dorso-laterally from the head (see harder prey such as crabs, beetles and snails (Bruton, 1979). Fig.·1) may indicate the avoidance of spatial interference with Although this species shows different kinds of foraging the buccal expansion system in course of the evolution. In this behaviours, including bottom feeding, surface feeding or group way, it is possible that the trade-off between biting and suction hunting, prey are generally captured by a combination of feeding performance, as suggested for other groups of fishes suction feeding and biting (Bruton, 1979; Van Wassenbergh et (Barel, 1983; De Visser and Barel, 1996), does not apply to al., 2004). The individuals used in the experiments (see further) Clariidae. were either aquarium-raised specimens obtained from the As suction feeding behaviour is thus maintained despite the Laboratory for Ecology and Aquaculture (Catholic University considerable increase in bite performance in several clariid of Leuven, Belgium) or specimens obtained from aquacultural facilities (Fleuren and Nooijen BV, Someren, The Netherlands). In contrast to C. gariepinus, G. typus and C. apus have bulging, hypertrophied, jaw adductors and a narrow skull roof (Fig.·1) (Cabuy et al., 1999; Devaere et al., 2001; Devaere et al., 2005). This increase in jaw muscle size, the reduction of the bony skull roof, and the development
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