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Prey Processing in the Siamese Fighting Fish (Betta Splendens)

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Prey Processing in the Siamese Fighting Fish (Betta Splendens) J Comp Physiol A DOI 10.1007/s00359-013-0819-5 ORIGINAL PAPER Prey processing in the Siamese fighting fish (Betta splendens) Nicolai Konow • Belma Krijestorac • Christopher P. J. Sanford • Renauld Boistel • Anthony Herrel Received: 12 November 2012 / Revised: 6 April 2013 / Accepted: 8 April 2013 Ó Springer-Verlag Berlin Heidelberg 2013 Abstract We studied prey processing in the Siamese oropharyngeal dentition surfaces to immobilize, reduce and fighting fish (Betta splendens), involving slow, easily process relatively large, tough or motile prey. Prey pro- observed head-bobbing movements, which were compared cessing outside the pharyngeal region has not been with prey processing in other aquatic feeding vertebrates. described for neoteleosts previously, but morphological We hypothesized that head-bobbing is a unique prey-pro- evidence suggests that relatives of Betta might use similar cessing behaviour, which alternatively could be structurally processing behaviours. Thus, our results suggest that and functionally analogous with raking in basal teleosts, or pharyngognathy did not out-compete ancestral prey-pro- with pharyngognathy in neoteleosts. Modulation of head- cessing mechanisms completely during the evolution of bobbing was elicited by prey with different motility neoteleosts. and toughness. Head-bobbing involved sustained mouth occlusion and pronounced cranial elevation, similar to Keywords Convergence Á Kinematics Á Oropharyngeal Á raking. However, the hyoid and pectoral girdle were Videofluoroscopy Á Nutritional physiology protracted, and not retracted as in both raking and phar- yngognathy. High-speed videofluoroscopy of hyoid Abbreviations movements confirmed that head-bobbing differs from other am Adductor mandibulae muscle known aquatic prey-processing behaviours. Nevertheless, bar Branchial arch remainders head-bobbing and other prey-processing behaviours con- bh Basihyal verge on a recurrent functional theme in the trophic ecol- bhh Horizontal movement of basihyal ogy of aquatic feeding vertebrates; the use of intraoral and bhv Vertical movement of basihyal bo Body cb Ceratobranchial Electronic supplementary material The online version of this article (doi:10.1007/s00359-013-0819-5) contains supplementary cbl Cleithrobranchial ligament material, which is available to authorized users. cv Craniovertebral joint gp Mandibular jaw gape expansion N. Konow Á B. Krijestorac Á C. P. J. Sanford j Jaw joint Department of Biology, Hofstra University, Hempstead, NY 11549, USA jp Jaw protrusion l Lower jaw Present Address: mnc Magnitude of cranial elevation & N. Konow ( ) mpg Magnitude of pectoral girdle protraction Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912, USA n Neurocranium e-mail: [email protected] nc Neurocranial elevation p Pectoral girdle R. Boistel Á A. Herrel pb Pharyngobranchial De´partement d’Ecologie et de Gestion de la Biodiversite´, UMR 7179 C.N.R.S/M.N.H.N., Case postale 55, pg Pectoral girdle movement 57 rue Cuvier, 75231 Paris Cedex 5, France ph Protractor hyoideus muscle 123 vertebrates (Table by three different feedingwide mechanisms variety in of aquaticventing prey-processing feeding its behaviours are escape,Prey governed and processing reducing it is prior critical to for digestion.Introduction A immobilizing prey, pre- l vncvpg Velocity of neurocranialv elevation Velocity of pectoralu girdle protraction Vomer TL Upper jaw Total length t susr Suspensorium ps Rostrum Parasphenoid prey-processing behaviours (Sanfordglossomorpha) have a and tongue-bite apparatus, Lauder salmonids used in raking (Salmoniformes)2010 and bony-tongueseralized gnathostome (Osteo- traitjaw apparatus (Lauder governs chewing, which likely is a gen- Claes andwinnowing De prey processing Vree (Liem pharyngognathy, which includesMost neoteleosts crushing, have a grinding pharyngeal1990 jaw and apparatus used for Grubich Betta splendens dentition, relative to aneoteleosts pharyngeal jaw with apparatus. et a al. different or reduced oropharyngeal (Taki larly by Resource 1) suggestflake that food. head-bobbing The is slowdisplayed observed and during regu- obvious feeding movements on (seeas Online more commercially delicate available andafter pellets. ingesting malleable This relatively large, behaviour2008 hard is and not brittle prey,of such the mostbehavioural frequently biology (Mabee traded and Trendler aquariumhas species a (Balboa well-described bony anatomy, is widely used in gesting that come from heavily modified rice paddockcomparative habitats, functional context. sug- head-bobbing has not been described or studied in a 123 0 CT Micro-computed tomography A popular model Neoteleost is the Siamese fighting fish, Descriptions of the trophic ecology of ; Konow et al. ; Konow and Sanford ). 2013 1978 Time-zero (cranial elevation onset) Betta 2000 Betta ). Yet, it is unknown if prey processing occurs in ; Berra Betta displays a peculiar head-bobbing behaviour , , [Anabantoidei (Ruber et al. owners feeding pellets to their pet. Still, 2003 feeds on small, soft-bodied larval insects 1 1981 ): the anterior-most mandibular or oral 2011 ; Wainwright 1991 ; Rainboth ). Some basal teleosts, including 2008a ; Drucker and Jensen , 1973 b 1989a ; Konow et al. 1996 1981 ; Aerts et al. , ). The idea of a 1996 ; Gintof et al. 2006 Betta 2006 ), and is one ; Gidmark )]. mainly 2008 1986 1991 1989 Betta ). ; ; , Table 1 Morphological, kinematics and muscle-activity pattern diagnostics of prey-processing systems in fishes; indicating structural and functional similarities between the intraoral jaw mechanism in Betta, and jaw mechanisms seen in other fish taxa Behaviour Jaw system Morphology Kinematics Muscle References activity Ventral jaw Dorsal jaw Other Cranial Pectoral girdle Mandible Head- Paraspheno- 5th ceratobranchiala 1st pharygo-branchiala Edentulous Elevation Protracted Occluded Early am, phb Liem (1963)a; Gosline (1985); Liem bobbing pharyngeal parasphenoid basihyal and Greenwood (1981)b in Betta Raking Tongue-bite Basihyal Vomer, parasphenoid CBL with Elevation Retracted Occluded Early am, ph Sanford and Lauder (1989; 1990)c; apparatus gill-arch Sanford (2001a), Sanford (2001b); processesc Hilton (2001)c; Camp et al. (2009); Konow and Sanford (2008a, b); Konow et al. (2008) Chewing Mandibular Mandible Premaxilla maxilla Level, slight Unaltered Cyclic Late am, ph Lauder (1981); Gintof et al. (2010) jaws elevation abduction- adduction Pharyngeal Pharyngeal 5th ceratobranchial 3rd pharyngobranchial Fused gill- Levele, Unalteredg,h Depressed N/Ai Liem (1973)e; Wainwright (1989b); d, e,f f,h f g processing jaw apparatus arches * slight (B7°) retracted passive Sibbing (1982) ; Aerts et al. (1986) ; J Comp Physiol A elevationf Claes and De Vree (1991)h; Wainwright (2006)d cbl cleithrobranchial ligament; am adductor mandibulae; ph protractor hyoideus a–h Specific works reporting the state of a given character i The pharyngeal jaw apparatus has distinct musculature relative to more anteriorly placed jaw apparatus, and thus an independent muscle-activity pattern, see Wainwright (2006) J Comp Physiol A nominal micro-invertebrate feeder using prey processing is modulation hypothesis, we fed Betta individuals with both puzzling. It suggests that head-bobbing may be a display blackworms and guppy fry, expecting that very different instead of a feeding behaviour, or that the lack of dietary demands would be imposed on the prey-processing data from undisturbed habitats has led to incorrect trophic behaviour by the contrasting toughness and motility of niche description for Betta. these prey types. Functional analyses of morphology and kinematics may Finally, we compared prey-processing morphology and help unravel behavioural, ecological and evolutionary links kinematics in Betta with available data from raking and (Wainwright 1991; Losey 1993). Therefore, we aimed at pharyngognath taxa, using the diagnostics of a tongue-bite comparing existing morphological data with high-speed apparatus developed earlier (Konow and Sanford 2008a, b) video and X-ray motion analyses of feeding apparatus and diagnostics of a pharyngeal jaw apparatus gathered kinematics. Our aim was to determine if Betta is capable of from the literature. We tested the hypotheses that oropha- capturing and processing large, tough and motile prey. ryngeal dentition morphology and prey-processing kine- Behavioural modulation, involving a predictable change matics in Betta were homologous with the tongue-bite in behavioural pattern as a response to changes in bio- apparatus and raking, or with the pharyngeal jaw apparatus physical stimuli, has been described for numerous feeding and pharyngognathy. Acceptance of the first morphology- behaviours. One consensus from feeding studies is that kinematics hypothesis would mean that raking prey pro- behavioural modulation reflects a heightened ecological cessing has evolved convergently in a derived neoteleost versatility compared with organisms with a stereotyped, or clade, in addition to the two basal teleost clades. Alterna- invariable behavioural response (Liem and Osse 1975; tively, acceptance of the second morphology-kinematics Frost and Sanford 1999). For example, differences in prey hypothesis would mean that Betta processes prey like other hardness or motility lead to modulation of raking prey neoteleosts. The alternative hypothesis was that prey pro- processing in some basal teleosts, but not in others (Frost cessing in Betta relies on a novel combination of mor- and Sanford 1999; Konow et al. 2008).
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