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Swim Bladder and Posterior Lateral Line Nerve of the Nurseryfish

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Swim Bladder and Posterior Lateral Line Nerve of the Nurseryfish JOURNAL OF MORPHOLOGY 260:193–200 (2004) Swim Bladder and Posterior Lateral Line Nerve of the Nurseryfish, Kurtus gulliveri (Perciformes: Kurtidae) Kent E. Carpenter,1* Tim M. Berra,2 and Julian M. Humphries Jr.3 1Department of Biological Sciences, Old Dominion University, Norfolk, Virginia 23529-0266 2Department of Evolution, Ecology and Organismal Biology, The Ohio State University, Mansfield, Ohio 44906 3Department of Geological Sciences, The University of Texas at Austin, Austin, Texas 78712 ABSTRACT The morphology of the swim bladder and and the inner ear as hearing “specialists.” They sug- inner ear of the nurseryfish, Kurtus gulliveri, appear gest that even without mechanical coupling the adapted for enhanced pressure wave reception. The sac- swim bladder can enhance hearing for “nonspecial- cule is enlarged and surrounded by very thin bone and two ists.” Yan et al. (2000), however, found no experi- large fontanelles that would present reduced resistance to mental evidence for enhanced hearing in nonspecial- pressure waves. The swim bladder is elaborate, with six ist fishes and suggested that the swim bladder may dorsolaterally projecting pairs of lobes that are tightly encased in ribs and an additional caudally projecting pair not serve as an accessory auditory organ in teleosts of lobes encased in the first hemal spine. The ribs and that lack mechanical coupling with the inner ear. musculature surrounding the swim bladder laterally are Hearing specializations help define several major very thin, so that four or five “rib windows” are readily teleostean lineages and are also found indepen- apparent on back-lit specimens. This swim bladder–rib dently in widely divergent taxonomic groups. A se- configuration would also present reduced resistance to ries of modified vertebrae that physically couples the pressure waves to enhance function as a peripheral audi- swim bladder to the inner ear forms the Weberian tory structure. However, high-resolution X-ray computed apparatus, which is a synapomorphy of otophysan tomography and dissection reveal no anterior projections fishes. This is thought to be a major factor in the of the swim bladder that could serve as a mechanical evolutionary success of this speciose clade of primar- coupling to the inner ear. The posterior lateral line nerve ily freshwater fishes that includes the Orders Cyp- is well developed and lies directly over the tips of the ribs riniformes (carps, minnows, loaches), Characi- encasing the swim bladder lobes. This nerve is not, how- ever, associated with a lateral line canal and a lateral line formes (characins), Siluriformes (catfishes), and canal is absent on most of the body. We hypothesize that Gymnotiformes (knifefishes). Auditory sensory en- the posterior lateral line nerve transmits mechanosensory hancement presumably is important in freshwater information from the swim bladder. J. Morphol. 260: habitats where turbidity impairs vision. Another 193–200, 2004. © 2004 Wiley-Liss, Inc. common form of hearing specialization in fishes is a rostral extension of the swim bladder toward the KEY WORDS: swim bladder; posterior lateral line nerve; inner ear (Popper and Fay, 1999). A form of this nurseryfish; mechanosensory; peripheral auditory struc- otophysic connection helps define the Clupeomorpha ture (herrings and anchovies). This mechanosensory spe- cialization potentially replaces the function of the lateral line, which is lacking on the body of most In addition to its role in buoyancy, the swim blad- clupeomorph fishes. Rostral extensions of the swim der is generally accepted as a simple resonating bladder also occur in euteleostean fishes including device and an accessory auditory organ in many fishes (Schellart and Wubbels, 1998). Gas in a swim bladder is compressible and the density difference Supplementary material for this article is avialable via the internet between gas and fluids presumably allows the swim at http://www.interscience.wiley.com/jpages/0362-2525/suppmat bladder to serve as an acoustic transformer capable of amplifying particle motion over a wide frequency Contract grant sponsor: National Geographic Society; Contract range (Hawkins, 1993). The swim bladder has been grant number: 6895-00; Contract grant sponsors: Columbus Zoo and Aquarium, Bioscience Productions (to T.M.B.), NSF; Contract grant shown to enhance mechanosensory function either number: NSF-0208675 (to J.M.H.). by coupling with the lateral line (Webb, 1998) or the inner ear. The inner ear of fishes detects mechanical *Correspondence to: Kent E. Carpenter, Department of Biological stimuli either by simple transmission of pressure Sciences, Old Dominion University, Norfolk, VA 23529-0266. waves through the braincase or with the aid of pe- E-mail: [email protected] ripheral auditory structures. Schellart and Wubbels (1998) classify fishes that utilize specialized me- chanical coupling devices between the swim bladder DOI: 10.1002/jmor.10184 © 2004 WILEY-LISS, INC. 194 K.E. CARPENTER ET AL. nocturnal squirrel fishes. These holocentrids have one of us (TMB). A map and description of the study varying degrees of contact between the swim blad- area are given by Berra (2003). Berra and Wedd der and the otic capsule and species with increased (2001) described the prawn, isopod, and fish diet of contact typically have a greater behavioral response nurseryfish. The gross anatomy and histology of the from an auditory stimulus (Coombs and Popper, male’s hook and skin were examined by Berra and 1979). Humphrey (2002). The integument in the cleft of the The typical habitat of nurseryfish is turbid coastal hook is devoid of secretory mucus and neurosensory rivers. In fishes found in this type of habitat the cells and is folded into crypts that extend into the lateral line is often well developed, presumably to dermis. This is considered a specialization that fa- augment vision as a form of sensory input. In the cilitates adhesion of the egg mass. Berra and Hum- nurseryfish, however, the lateral line canal is re- phrey (2002) speculated that the highly vascularized stricted to the anterior part of the body just above dermis engorges with blood and helps clamp the egg the pectoral fin. The posteriormost extent of the mass in place. Eggs and pre- and postflexion larvae lateral line canal ends at a vertical near the origin of were described by Berra and Neira (2003) who noted the dorsal fin. Beaufort (1914) pointed out that the a prominent, inflated swim bladder in post-yolk-sac bones of the neurocranium are very thin and that young. The larvae are pelagic and hatch at about 5 the otic bulla is bordered both dorsally and laterally mm body length. They leave the plankton at about by fontanelles. However, he did not point out that 25 mm standard length. Berra (2003) compared the these morphological features could theoretically fa- meristics and morphometrics of Kurtus gulliveri and cilitate direct near field mechanosensory perception K. indicus, remarked on the unusual “rib windows,” of the inner ear. Beaufort (1914) also described the and provided a color description and map of K. gul- oddly shaped dorsolaterally projecting lobes of the liveri distribution. swim bladder and their encasement and close con- The purpose of this article is to illustrate the gross nection with bizarre-shaped ribs. He did not detail morphology of the swim bladder, to describe the the overall shape of the swim bladder or speculate association of posterior lateral line nerve (Puzd- on the potential auditory function of this arrange- rowski, 1989) with the swim bladder, and to specu- ment. We hypothesized that the unique swim blad- late on the mechanosensory enhancement provided der morphology found in nurseryfish may serve as a by this arrangement. Our study was assisted by peripheral auditory structure and could help com- scanning with high-resolution X-ray computed to- pensate for the lack of an extensive lateral line canal mography (HRCT) that revealed the structure and on the body. arrangement of the ribs, swim bladder, and otoliths. Kurtus gulliveri is found in coastal rivers of south- ern New Guinea and northern Australia, and its smaller congener, K. indicus, occurs from India to MATERIALS AND METHODS Borneo (Berra, 2001). These two species constitute the Kurtidae and the only family within the perci- Nurseryfish, Kurtus gulliveri, were collected by gill nets from the Adelaide River during April–November 2001, placed on ice, form suborder Kurtoidei (Nelson, 1994). Kurtus gul- then fixed in 10% formalin (Berra, 2003) or retained fresh for liveri is notable for its unusual mode of parental disarticulated skeletal preparations. Fixed material was pre- care. The male carries an egg mass attached to a served in 70% ethanol. Disarticulated skeletal material was pre- supraoccipital hook. This assembly resembles a clus- pared by leaving fresh specimens in water outside in tropical ambient temperatures for several weeks, allowing soft tissues to ter of tiny grapes on the fish’s head, which resulted decay. Fixed specimens were cleared and counterstained for bone in the common name of nurseryfish applied to this and cartilage following the method of Dingerkus and Uhler “forehead brooding” species (Balon, 1975). This re- (1977). Opercular bones and the pectoral girdle were removed markable system was first reported by Weber (1910, from cleared and stained specimens on the right side to expose 1913). Guitel (1913) described the early-stage eggs the area between the swim bladder and the neurocranium. Soft tissue was viewed in cleared and stained specimens by reimmers- of Weber’s specimen. Beaufort (1914) diagrammed ing the specimen in 70% ethanol. Soft tissues were also viewed in the skeleton including the unusual expanded ribs whole preserved specimens by dissecting away opercular bones, surrounding the lobed swim bladder and discussed the pectoral girdle, lateral musculature, and associated perito- various aspects of soft anatomy. Until recently, al- neum. Osteology and swim bladder morphology were also exam- ined on whole specimens using HRCT. The specimens were most nothing has been published on the biology of scanned at the HRCT Facility at the University of Texas at this species since these 90-year-old articles.
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