Morphology and Function of the Feeding Apparatus of the Lungfish, Lepidosiren Paradoxa (Dipnoi)
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JOURNAL OF MORPHOLOGY 187:81-108 (1986) Morphology and Function of the Feeding Apparatus of the Lungfish, Lepidosiren paradoxa (Dipnoi) W. E. BEMIS AND GEORGE V. LAUDER Department of Anatomy, University of Chicago, Chicago, Illinois ABSTRACT The feeding mechanism of the South American lungfish, Lep idosiren paradoxa retains many primitive teleostome characteristics. In partic- ular, the process of initial prey capture shares four salient functional features with other primitive vertebrates: 1) prey capture by suction feeding, 2) cranial elevation at the cranio-vertebral joint during the mouth opening phase of the strike, 3) the hyoid apparatus plays a major role in mediating expansion of the oral cavity and is one biomechanical pathway involved in depressing the mandible, and 4)peak hyoid excursion occurs after maximum gape is achieved. Lepidosiren also possesses four key morphological and functional specializa- tions of the feeding mechanism: 1) tooth plates, 2) an enlarged cranial rib serving as a site for the origin of muscles depressing the hyoid apparatus, 3) a depressor mandibulae muscle, apparently not homologous to that of amphibi- ans, and 4) a complex sequence of manipulation and chewing of prey in the oral cavity prior to swallowing. The depressor madibulae is always active during mouth opening, in contrast to some previous suggestions. Chewing cycles include alternating adduction and transport phases. Between each adduction, food may be transported in or out of the buccal cavity to position it between the tooth plates. The depressor mandibulae muscle is active in a double-burst pattern during chewing, with the larger second burst serving to open the mouth during prey transport. Swallowing is characterized by prolonged activity in the hyoid constrictor musculature and the geniotho- racicus. Lepidosiren uses hydraulic transport achieved by movements of the hyoid apparatus to position prey within the oral cavity. This function is analagous to that of the tongue in many tetrapods. A key event in the evolution of land verte- more distant outgroup (Schultze and Trueb, brates from fishes was the transition from '81), lungfshes are the closest living out- aquatic suction feeding to terrestrial feeding group of tetrapods, Latimeria probably being with the tongue and jaws. This transition more distantly related to tetrapods than pre- involved numerous major changes in the viously supposed (Miles, '77; Wiley, '79; Ro- feeding mechanism, such as the evolution of sen et al., '81). As such, dipnoans are in a novel mechanisms for acquiring food, han- unique position to offer insight into the evo- dling it in the oral cavity, and swallowing lution of tetrapod feeding systems. At the the processed food (Bramble and Wake, '85). same time, members of the radiation of lung- Although much has been written about the fishes, distinct from its first appearance in fish--amphibiantransition, little information the lower Devonian, have diverged exten- exists on the feeding mechanics of the Dipnoi sively from the common primitive body plan or lungfshes, one of the most important liv- that lungfishes and tetrapods shared. The ing groups relevant to the origin of terres- extant lungfishes are in some respects poor trial feeding (Thomson, '69). The phylogen- models of phylogenetically primitive lung- etic position of lungfishes makes this group critical to our understanding of vertebrate Dr. Bemis' present address is Department of Zoology, Univer- evolution. Whether lungfishes are regarded sity of Massachusetts, Amherst, MA 01003-0027. as the sister group of tetrapods (Rosen et al., Dr. Lauder's present address is Department of Developmental '81) or whether they are considered to be a and Cell Biology, University of California, Irvine CA 92717. 0 1986 ALAN R. LISS, INC. 82 W.E. BEMIS AND G.V. LAUDER fishes. We know this, because their excellent mammalian mastication. A final goal of this fossil record documents extensive morpholog- paper will thus be to discuss some of these ical change during their evolution (Bemis, convergent features, particularly the lingual '84b). For example, early in their history, transport system typically used by tetrapods lungfishes exhibited much evolutionary div- and the hydraulic transport system used by ersification and specialization in the feeding lungfkhes. apparatus, and two distinct groups-one with specialized tooth plates and the other show- MATERIALS AND METHODS ing periodic growth and shedding of denti- Animals and diet cles-can be recognized (Campbell and Bar- Nine individual Lepidosiren paradoxa ob- wick, '83). tained from commercial dealers were avail- In this paper, we provide the first cinema- able for this study. The five specimens used tographic and electromyographicstudy of the for experiments ranged in size from 15 cm feeding system of any dipnoan. The subject total length (TL) to 20 cm TL. Individuals of our study is the South American lungfish, were housed in 20-liter aquaria held at ap- Lepidosiren paradoxa. Lepidosiren and the proximately 26 degrees C. Animals were closely related African lungfishes, Protopte trained to feed readily on pieces of earth- rus spp., are members of a clade that is dis- worm (Lumbricus).A special training period tinct in many respects from the Australian to accustom the animals to feeding under the lungfish, Neoceratodus. Thomson ('69) pro- bright movie lights began one month prior to vided a general discussion of dipnoan food the start of filming. Individuals were starved and feeding systems, and concluded that the for up to two weeks prior to either filming manner of feeding in all three genera is sim- sessions or electromyographic studies. Large ilar. In the only detailed examination of the African lungfish, Protopterus aethwpicus, are feeding mechanics of living lungfishes, Per- known to feed extensively on molluscs, al- kins ('72) based conclusions about muscle though smaller individuals consume a diver- function solely on dissections. Most research sity of both hard and soft bodied inverte- on the functional morphology of lungfishes brates (Corbet, '61). Sparse ecological data has focused on respiration and circulation, available for Lepidosiren is inconclusive con- such as the electromyography of respiration cerning dietary specialization, though it in Protopterus (McMahon, '691, cineradiogra- seems likely that they are opportunistic om- phy of air breathing in Lepidosiren (Bishop nivores. Carter and Beadle ('30) maintained and Foxon, '68), and functional anatomy and young specimens on a diet of earthworms, physiology of lungfish hearts and circulatory prepared (presumably shell-less) snails, and systems (e.g., Johansen and Hanson, '68). plant material. They considered plant mate- The major goal of our study was to describe rial to be especially important, and stated and analyze the feeding of Lepidosiren and that only a few potential prey items-worms, use this information to identify anatomical insects, and insect larvae-were available in and functional features of the feeding system the water where the fish were taken. On the that are primitive to dipnoans. These primi- other hand, Lankester (1896),citing the field tive features are then compared to those observations of Bohls, stated that Lepidosi- previously identified in the feeding systems ren feeds chiefly on the hard-shelled snail of other lower vertebrates (e.g., ray-finned Ampullaria, and that plant material may be fishes, coelacanths, and salamanders). Com- ingested by accident. parison allows us to recognize which features of the vertebrate feeding mechanism are A natorny phylogenetically common to all of these lin- Gross morphological features of the feeding eages, which features are common to tetra- apparatus (osteology, arthrology, and myol- pods and lungfishes, and which are special- ogy) were examined by dissection using a izations limited to the Dipnoi. A second goal Zeiss IVb dissecting microscope. A camera was to provide a detailed functional analysis lucida attachment was used to prepare the of the tooth plates, which are the major spe- figures from dissected specimens and cleared cialization of the feeding mechanism of ex- and stained specimens. Three individuals tant lungfkhes. Unlike the vast majority of were cleared and stained (for both cartilage fishes, lungfishes process food items using a and bone) following procedures modified from marginally placed dental apparatus, with Wassersug ('76) and Dingerkus and Uhler movements that are broadly convergent to ('77). In addition, prepared skeletons were FEEDING MECHANICS OF LUNGFISH 83 used to examine osteological details. Both both the lower jaw and the hyoid apparatus. dry and cleared and stained material was It was measured as the perpendicular dis- also available for Protopterus. tance from a line drawn between the hyoid The serially sectioned head of a single in- and the lower lip to the most indented point dividual prepared for an earlier study (Be- on the lower jaw between the two end points. mis, ’84a) was available for analysis. Briefly, Together, these two measurements provide a this specimen was fixed in 5% neutral buf€- qualitative estimate of both the length and ered formalin, embedded in low viscosity ni- strength of the adduction phase of chewing. trocellulose (type RS 1/2, Hercules Inc., To aid in interpreting electromyographic Wilmington, Delaware), and serially cross recordings, simultaneous video recordings sectioned at 30 pm. Most sections were were made of feeding behavior. A Panasonic stained with Ehrlich’s