A Functional-Morphological Study on the Attachment, Respiration and Feeding Mechanisms in Balitorinae (Balitoridae, Teleostei)

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A Functional-Morphological Study on the Attachment, Respiration and Feeding Mechanisms in Balitorinae (Balitoridae, Teleostei) Faculty of Sciences Department of Biology Research group: Evolutionary Morphology of Vertebrates Academic year 2012-2013 A functional-morphological study on the attachment, respiration and feeding mechanisms in Balitorinae (Balitoridae, Teleostei) De Meyer Jens Supervisor: Dr. Tom Geerinckx Thesis submitted to obtain the degree of Tutor: Dr. Tom Geerinckx Master in Biology II © Faculty of Sciences – Evolutionary Morphology of Vertebrates Deze masterproef bevat vertrouwelijk informatie en vertrouwelijke onderzoeksresultaten die toebehoren aan de UGent. De inhoud van de masterproef mag onder geen enkele manier publiek gemaakt worden, noch geheel noch gedeeltelijk zonder de uitdrukkelijke schriftelijke voorafgaandelijke toestemming van de UGent vertegenwoordiger, in casu de promotor. Zo is het nemen van kopieën of het op eender welke wijze dupliceren van het eindwerk verboden, tenzij met schriftelijke toestemming. Het niet respecteren van de confidentiële aard van het eindwerk veroorzaakt onherstelbare schade aan de UGent. Ingeval een geschil zou ontstaan in het kader van deze verklaring, zijn de rechtbanken van het arrondissement Gent uitsluitend bevoegd daarvan kennis te nemen. All rights reserved. This thesis contains confidential information and confidential research results that are property to the UGent. The contents of this master thesis may under no circumstances be made public, nor complete or partial, without the explicit and preceding permission of the UGent representative, i.e. the supervisor. The thesis may under no circumstances be copied or duplicated in any form, unless permission granted in written form. Any violation of the confidential nature of this thesis may impose irreparable damage to the UGent. In case of a dispute that may arise within the context of this declaration, the Judicial Court of© All rights reserved. This thesis contains confidential information and confidential research results that are property to the UGent. III IV Index 1. Introduction 1 2. Materials and Methods 6 2.1 Specimens 6 2.2 Kinematics 7 A. Recordings 7 B. Digitization and analysis 8 2.3 Morphology 9 A. Clearing and staining 9 B. Serial sections 9 C. Computed tomography 10 3. Results 11 3.1 Osteology 11 A. Osteology of Beaufortia leveretti 11 Neurocranium 11 Ethmoid region and infraorbital series 14 Hyopalatine arch and opercular series 15 Lower jaw 16 Hyoid arch 17 Pectoral girdle 18 B. Osteology of Sewellia lineolata and Pseudogastromyzon myersi 19 C. Osteology of Botia marcracantha, B. loachata and Lefua costata 21 3.2 Myology 22 3.3 Kinematics 29 A.1 Respiration - timing 29 A.2 Respiration - movement 34 B.1 Feeding - timing 37 B.2 Feeding - movement 38 4. Discussion 40 4.1 Osteological variation 40 4.2 Feeding and respiration 44 4.3 Attachment 49 4.4 Movement 54 5. Conclusion 55 6. Acknowledgements 57 7. Summary – Samenvatting 58 7.1 Summary 58 7.2 Samenvatting 61 8. References 64 V VI 1. Introduction Functional morphology studies the morphology of structures such as muscles and bones and relates this to their function. To understand how morphology is linked to their functioning, it is useful to investigate specialized species. Specialization has no strict definition and is used in several articles with a different meaning. The existing definitions can be placed in three main categories, depending on their point of view: ecological, mechanistic and evolutionary specialization, respectively (Ferry-Graham et al. 2002). These definitions have in common that a specialist can obtain certain resources (food, shelter, …) more easily than a generalist, which uses a wide range of resources. Specialization is most easily observed in species that have well pronounced or extreme structures. As stated by Adriaens & Herrel (2009), many insights of biological problems can be obtained by studying extreme morphologies. These studies can not only provide us information about how a species adapts to its specific niche, but also allow us to get a better understanding of how natural selection works. Selection mostly favors average phenotypes in most environments, because these can be highly variable (Ridley 2003). However, both disruptive and directional selection allows well pronounced morphologies to develop in the range of all possible phenotypes (Santos 1996, Benkman 2003, Bolnick 2004). These morphologies are thus only selected when they cause a fitness benefit in their ecological environment (Ridley 2003). Studies focused on extreme specializations range from the extreme length of viper fangs (Cundall 2009), over the long ballistic tongue of the Hydromantes (Plethodonthidae) (Deban & Wake 1997), to the specializations of the snout of seahorses (Roos et al. 2009, Leysen et al. 2011). Teleost fishes are the most species-rich and morphologically diverse group of vertebrates (Nelson 2006, Wainwright 2006, Mehta 2009). Because of this diversity, teleosts have been used in many morphological and ecological studies, especially in studies related to feeding (e.g., Lauder 1983, Clifton & Motta 1998, Grubich 2003, Waltzek & Wainwright 2003, Janovetz 2005). 1 The tropical Asian rivers contain very rich and diverse fish communities (Lowe-McConnell 1987, Dudgeon 1999, 2000), but ecological research on these species, especially those of low commercial value, is most often neglected (Jacob & Suryanarayanan 1990, de Silva 1991, Roberts 1993, Martin-Smith 1998a, Dudgeon 2000). Fishes inhabiting fast-flowing rivers need specialized modifications in their morphology to prevent themselves from being swept away by the strong water currents. These modifications are mostly related to the formation of adhesive structures at the anterior end of the ventral body side and on the fins. Hora (1922, 1930) already studied a variety of torrential fishes in function of their adaptations to life in fast currents and rocky substrates. He superficially described the attachment capabilities of Balitoridae, formerly known as Homalopteridae (Hora 1932, Kottelat 1988, ICZN 1993). Balitoridae, commonly called river or hill stream loaches, are a diverse group of around 600 species, divided over 59 genera (Nelson 2006). They are native to Eurasia and Africa, with the highest diversity in Asia (Nelson 2006) and still new species are being described (Gu & Zhang 2012, Lokeshwor & Vishwanath 2012, Yang et al. 2012). A fair number of these 600 species are nowadays found in aquarium trade. Balitoridae are subdivided in two subfamilies, Balitorinae and Nemacheilinae (Sawada 1982, Nelson 2006; Fig 3). The monophyly of the family, however, has been questioned (Slechtova et al. 2007), and some researchers prefer the separate families Nemacheilidae and Balitoridae (Conway 2011, Staab et al. 2012). As stated before, there is almost no information about the ecology of Balitoridae sensu lato (Dudgeon 2000), because most studies are related to taxonomy, phylogeny or external morphology (Hora 1930, Kottelat 1988, Roberts 1993, Tang et al. 2006, 2011). Most Balitoridae are primarily herbivorous, feeding on algae, but they are also dependent on animal food, such as benthic macro-invertebrates and aquatic insects (Mantel et al. 2004, Ward-Campbell et al. 2005, Herder & Freyhof 2006, Beamish et al. 2008). Martin-Smith (1998a) found that in Malaysia the riffles in rivers are dominated by Balitoridae. Riffles are associated with high velocity and turbulence and to live in such circumstances, Balitoridae developed certain specializations. 2 This study focuses on the subfamily Balitorinae, which is characterized by an anteriorly flattened body and restricted gill openings, placed above the pectoral fins. They have a permanent ventrally oriented mouth. To prevent being washed away by the fast currents, they have developed a form of sucking ability. The pectoral and pelvic fins are inserted horizontally and have been expanded so they can be used as sucker-like adhesive organs (Yang & Dudgeon 2009). These fins allow them to cling to rocks (Banister et al. 1998). Figure 1: Left: Distribution of the investigated species. Right: Pictures of their natural habitat1. For this research, four species were selected that are characterized by pectoral fins overlapping the pelvic fins and by strongly reduced to absent barbels. Sewellia lineolata and Beaufortia leveretti exhibit a more dorsoventrally flattened body, whereas the body of Pseudogastromyzon myersi and Gastromyzon punctulatus (Fig 2) is less flattened. These fishes are found in fast-flowing rivers in different areas of Asia (Fig 1). By studying these fishes, a more detailed description can be made about the specific attachment mechanisms. By comparing these mechanisms with those of other species using attachment, it is possible to determine if there are multiple solutions for suction behavior or if convergent evolution has taken place. This study also gives attention to the feeding and respiration structures and mechanisms in Balitorinae to find out if there are trade-offs between suction behavior on the one hand and feeding and breathing on the other hand. 1 Source: www.loaches.com/articles/sewellia-lineolata-natural-habitat-and-how-they-get-to-our-aquariums 3 Therefore the main aims are: 1. Describing the internal morphology, with the aim of identifying the anatomical structures and muscles that are used during attachment, respiration and feeding. More than one species is being studied to detect any structural variation present between species. 2. Understanding how structures such as fins and head parts are acting during feeding and non-feeding stages
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