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The Highly Derived Larval Anatomy of Occidozyga Baluensis (Boulenger, 1896), an Obligate Carnivorous Tadpole

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The Highly Derived Larval Anatomy of Occidozyga Baluensis (Boulenger, 1896), an Obligate Carnivorous Tadpole Zoomorphology (2014) 133:321–342 DOI 10.1007/s00435-014-0226-7 ORIGINAL PAPER Extreme tadpoles II: the highly derived larval anatomy of Occidozyga baluensis (Boulenger, 1896), an obligate carnivorous tadpole Alexander Haas • Jana Pohlmeyer • David S. McLeod • Thomas Kleinteich • Stefan T. Hertwig • Indraneil Das • Daniel R. Buchholz Received: 28 November 2013 / Revised: 21 February 2014 / Accepted: 25 February 2014 / Published online: 21 March 2014 Ó Springer-Verlag Berlin Heidelberg 2014 Abstract Tadpoles of Occidozyga species have been arrangement of structures that form the buccal cavity, we reported to be carnivorous, feeding on insects and other hypothesize that suction feeding utilizing strong negative tadpoles. We present photographic evidence for the pre- pressure is employed by this species. Furthermore, we viously undocumented larval feeding behavior in O. bal- propose that force, rather than speed, is the main charac- uensis. Furthermore, we present a detailed anatomical teristic of their feeding. The unique features of the study description of the skull, cranial musculature, and gross gut species substantially expand the known morphospace for morphology based on three-dimensional reconstructions tadpoles, particularly among the Acosmanura (Pelobatoi- from serial sections and lCT imagery. The cranial anatomy dea, Pelodytoidea, and Neobatrachia). Except for Micro- of larval O. baluensis is highly derived in many characters, hylidae, acosmanurans previously described possess with respect to taxa outside the genus Occidozyga, most limited innovative larval morphologies. Larval carnivory notably the palatoquadrate and hyobranchial apparatus, that has evolved convergently several times in distant anuran play a major role in tadpole feeding. A large larval stomach clades and shows structural, behavioral, and functional was present in the specimens examined, indicative of a differences in the known examples. macrophagous carnivorous mode of feeding. Because of the relatively small oral orifice, relatively large-sized food Keywords Lissamphibia Á Anura Á Dicroglossidae Á items found in the larval stomach, and the tunnel-like Carnivory Á Cranium Á Larval stomach Communicated by A. Schmidt-Rhaesa. A. Haas (&) Á J. Pohlmeyer S. T. Hertwig Biozentrum Grindel und Zoologisches Museum Hamburg, Naturhistorisches Museum der Burgergemeinde Bern, Martin-Luther-King-Platz 3, 20146 Hamburg, Bernastrasse 15, 3005 Bern, Switzerland Germany e-mail: [email protected] e-mail: [email protected] J. Pohlmeyer I. Das e-mail: [email protected] Institute of Biodiversity and Environmental Conservation, Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, D. S. McLeod Malaysia University of Kansas Biodiversity Institute, 1345 Jayhawk e-mail: [email protected] Boulevard, Lawrence, KS 66045-7561, USA e-mail: [email protected] D. R. Buchholz Department of Biological Sciences, University of Cincinnati, T. Kleinteich 711A Rieveschl Hall, 312 Clifton Ct., Cincinnati, OH 45221, Functional Morphology and Biomechanics, Christian-Albrechts- USA Universita¨t Kiel, Am Botanischen Garten 1–9, 24098 Kiel, e-mail: [email protected] Germany e-mail: [email protected] 123 322 Zoomorphology (2014) 133:321–342 Abbreviations that engulf large food items in toto have been classified 3D Three-dimensional macrophagous (Altig and Johnston 1989) or megalopha- cart. Cartilago gous (Ruibal and Thomas 1988). We prefer the former for. Foramen term, implying an uptake of food items that are signifi- lev. Levator cantly larger than food items in generalized opportunisti- m. Musculus cally feeding tadpoles and large relative to the tadpole’s mand. Mandibulae own size. Macrophagy and carnivory have each been used proc. Processus to define tadpole guilds (Altig and Johnston 1989), despite prof. Profundus the independence of these terms (size vs. kind of food). In most known cases, macrophagous tadpoles are carnivores, but macrophagy can be combined with herbivory (macro- phagous herbivore) if large plant parts are swallowed as Introduction suggested for some Dendropsophus (Wassersug 1980). Herein, we use carnivory as an inclusive category for both Most anuran amphibian species have complex life cycles, macrophagous carnivores and carnivores that are not where distinct aquatic and terrestrial stages are connected macrophagous. by a short metamorphic phase that dramatically restruc- Obligate carnivorous tadpoles are rare. The macropha- tures the body. The exploitation of available food resour- gous carnivorous larva of the Neotropical Lepidobatrachus ces, with moderate probability of mortality in two different species (Ceratophryidae) is a suction feeder that can engulf life phases, can be considered the primary advantage of a and swallow large prey, such as tadpoles of other species complex life cycle (Harris 1999 and references therein). It and conspecifics (Cei 1968; Ulloa Kreisel 2002; Fabrezi is common in the literature to label tadpoles as herbivo- and Lobo 2009). Related to this mode of feeding, and in rous, because many species take up algae and other plant contrast to almost all other anuran larvae, the snout is very materials, but the true food items that tadpoles ingest and broad and the oral orifice is wide in larval Lepidobatra- assimilate across taxonomic groups have not been inves- chus; beaks are reduced, and keratodonts are absent (Ruibal tigated on a broad scale (Altig et al. 2007). Some studies and Thomas 1988; Altig and Johnston 1989; Haas 2003). suggest that animal matter and predation play a more Additionally, derived anatomical character states related to important role in tadpole feeding and that tadpoles occupy this mode of feeding can be identified in the cranium, a higher level in the aquatic food web than previously musculature, buccal structure, and gut of this species thought (Petranka and Kennedy 1999; Vera Candioti (Ruibal and Thomas 1988; Lavilla and Fabrezi 1992; Haas 2007). Because tadpoles with beaks and keratodonts are 2003; Vera Candioti 2007; Fabrezi and Quinzio 2008; often observed eating dead siblings or carrion in laboratory Ziermann et al. 2011). The closely related Ceratophrys and natural settings, it is suspected that many supposedly cranwelli and C. ornata have carnivorous larvae as well, herbivorous species may turn out to be opportunistic but they actively attack tadpoles of sympatric species by omnivores upon closer investigation (McDiarmid and Altig holding their prey with their mouthparts and biting off 1999; Altig et al. 2007). Food items usually are small, flesh. Their jaw and hyoidean musculature are strongly generated with larval beaks or not, and are flushed into the developed (Vera Candioti 2005; Fabrezi and Quinzio 2008; mouth with water current produced by the hyal pumping Natale et al. 2011). Independent evolution of masticatory mechanism (de Jongh 1968; de Jongh and Gans 1969; carnivorous feeding, accompanied by large larval beaks Gradwell 1972). In the bucco-branchial cavity, branchial bearing projections, hypertrophied jaw muscles, and pred- filter epithelia and mucus secretions trap the food items atory behavior, has been documented in Hoplobatrachus (Dodd 1950; Kenny 1969). The presence of mucus (Grosjean et al. 2004) and Spea (Bragg 1956, 1964; Fox entrapment and facultative suspension feeding is consid- 1990; Pfennig 1992). Interestingly, tadpoles of the genus ered apomorphic for the Anura (Sokol 1975; Haas 2003). Spea are facultatively carnivorous, where the presence of This food entrapment and filtering allows the exploitation fairy shrimp early in premetamorphosis induces a carnivore of a wide variety of food resources from small, unicellar morph characterized by not only larger jaw muscles and organisms, floating algae, bacteria, and fungi, to rasping altered larval beak shape but also larger overall body size, leaves, feeding on carrion, and sifting through detritus at shorter intestine length, and shorter larval period (Pomeroy pond bottoms (Altig et al. 2007). 1981; Pfennig 1992). Macrophagous larvae of the Den- Obligate or high degrees of carnivory, herein defined as dropsophus microcephalus group (some species have her- feeding exclusively or predominantly on metazoan food bivorous and some have carnivorous larvae) have moderate sources, have been confirmed only in tadpoles of a few frog jaws and lower lips that form a suction tube (Wassersug genera (Altig and McDiarmid 1999). Carnivorous tadpoles 1980; Vera Candioti et al. 2004; Vera Candioti 2007). 123 Zoomorphology (2014) 133:321–342 323 Tadpoles of Hymenochirus, and presumably Pseudohy- Table 1 Materials examined of Occidozyga baluensis larvae menochirus, demonstrate a unique form of carnivory that examined involves biomechanics convergent with teleosts to create Field/ Catalog Head-body Preparation/remarks suction for feeding upon small live prey (Sokol 1962; lab length in Deban and Olson 2002). Oophagy as another form of number mm carnivory has been reported from pond species (Petranka #492P ZMH A – None; photos of living specimen and Kennedy 1999) and phytothelm-breeding species; in 13117 some of the latter, nutritive unfertilized eggs from the #492-1 ZMH A 6.05 Histological serial sections mother are consumed by offspring (Crump 1992; Jungfer 13112 1996). Reduction in intraoral epithelial structures, such as #492-2 ZMH A 6.15 Histological serial sections branchial food traps and filter rows, has been reported in 13111 the carnivorous larva of Dendropsophus, Lepidobatrachus #492-3 ZMH A 5.63 Histological serial
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