Laterophysic Connection Research Articles

Acoustic Communication in Butterflyfishes: Anatomical Novelties, Physiology, Evolution, and Behavioral Ecology.

Coral reef fishes live in noisy environments that may challenge their capacity for acoustic communication. Butterflyfishes (Family Chaetodontidae) are prominent and ecologically diverse members of coral reef communities worldwide. The discovery of a novel association of anterior swim bladder horns with the lateral line canal system in the genus Chaetodon (the laterophysic connection) revealed a putative adaptation for enhancement of sound reception by the lateral line system and/or the ear. Behavioral studies show that acoustic communication is an important component of butterflyfish social behavior. All bannerfish (Forcipiger, Heniochus, and Hemitaurichthys) and Chaetodon species studied thus far produce several sound types at frequencies of <1 to >1000 Hz. Ancestral character state analyses predict the existence of both shared (head bob) and divergent (tail slap) acoustic behaviors in these two clades. Experimental auditory physiology shows that butterflyfishes are primarily sensitive to stimuli associated with hydrodynamic particle accelerations of ≤500 Hz. In addition, the gas-filled swim bladder horns in Chaetodon are stimulated by sound pressure, which enhances and extends their auditory sensitivity to 1700-2000 Hz. The broadband spectrum of ambient noise present on coral reefs overlaps with the frequency characteristics of their sounds, thus both the close social affiliations common among butterflyfishes and the evolution of the swim bladder horns in Chaetodon facilitate their short-range acoustic communication. Butterflyfishes provide a unique and unexpected opportunity to carry out studies of fish bioacoustics in the lab and the field that integrate the study of sensory anatomy, physiology, evolution, and behavioral ecology.

Diversity and evolution of sound production in the social behavior ofChaetodonbutterflyfishes

Fish produce context-specific sounds during social communication, but it is not known how acoustic behaviors have evolved in relation to specializations of the auditory system. Butterflyfishes (family Chaetodontidae) have a well-defined phylogeny and produce pulsed communication sounds during social interactions on coral reefs. Recent work indicates that two sound production mechanisms exist in the bannerfish clade and that other mechanisms are used in the Chaetodon clade, which is distinguished by an auditory specialization, the laterophysic connection (LC). Here, we determine the kinematic action patterns associated with sound production during social interactions in four Chaetodon subgenera and the non-laterophysic fish Forcipiger flavissimus. Some Chaetodon species share the head bob acoustic behavior with F. flavissimus, which along with other sounds in the 100-1000 Hz spectrum, are probably adequate to stimulate the ear, swim bladder or LC of a receiver fish. In contrast, only Chaetodon species produced the tail slap sound, which involves a 1-30 Hz hydrodynamic pulse that is likely to stimulate the receiver's ear and lateral line at close distances, but not the swim bladder or LC. Reconstructions of ancestral character states appear equivocal for the head bob and divergent for the tail slap acoustic behaviors. Independent contrast analysis shows a correlation between sound duration and stimulus intensity characters. The intensities of the tail slap and body pulse sounds in Chaeotodon species are correlated with body size and can provide honest communication signals. Future studies on fish acoustic communication should investigate low-frequency and infrasound acoustic fields to understand the integrated function of the ear and lateral line, and their evolutionary patterns.

Sound pressure enhances the hearing sensitivity of Chaetodon butterflyfishes on noisy coral reefs

Butterflyfishes are conspicuous members of coral reefs that communicate with acoustic signals during social interactions with mates and other conspecifics. Members of the genus Chaetodon have a laterophysic connection (LC) - a unique association of anterior swim bladder horns and the cranial lateral line - but the action of the LC system on auditory sensitivity is unexplored. Here, we show in baseline auditory evoked potential threshold experiments that Forcipiger flavissimus (which lacks swim bladder horns and LC) is sensitive to sound tones from 100 Hz up to 1000 Hz, and that thresholds for three species of Chaetodon are 10-15 dB lower, with extended hearing ranges up to 1700-2000 Hz. The relatively high thresholds to sound pressure and low pass response near 500 Hz for all four species are consistent with a primary sensitivity to hydrodynamic particle acceleration rather than sound pressure. Deflation of the swim bladder in F. flavissimus had no measurable effect on auditory sensitivity. In contrast, displacement of gas from the swim bladder horns in Chaetodon multicinctus and Chaetodon auriga increased thresholds (decreased sensitivity) by 5-20 dB, with the greatest effect at 600 Hz. The evolution of swim bladder horns associated with the LC system in Chaetodon species has increased hearing sensitivity through sound pressure transduction in the frequency bands used for social acoustic communication. The close affiliative behaviors that are common in Chaetodon species and other butterflyfish facilitate sound perception and acoustic communication at close distances relative to the high background noise levels found in their natural reef environment.

Development of the ear, hearing capabilities and laterophysic connection in the spotfin butterflyfish (Chaetodon ocellatus)

The ontogeny of the ear, swim bladder and laterophysic connection was investigated in the spotfin butterflyfish, Chaetodon ocellatus in order to determine how the development of the laterophysic connection (a Chaetodon synapomorphy) is correlated with ontogenetic changes in the hearing capabilities in these abundant and ecologically important coral reef fishes. Histological and cleared and stained material revealed that the medial opening in the lateral line canal in the supracleithrum (which defines the laterophysic connection), an inflated physoclistous swim bladder, and the three otolithic organs are already present in the smallest individuals examined (7–15 mm SL). The medial opening in the supracleithrum increases in size and the cylindrical swim bladder horns form after the loss of the head plates characteristic of the tholichthys stage, in individuals ≥29 mm SL. The three sensory maculae of the ear increase in size, and the shape of the sacculus changes most dramatically with fish growth; hair cell density is highest in the utriculus. Physiological analysis of the reponse to sound pressure showed that larval and juvenile C. ocellatus had a hearing sensitivity peak at 100–200 Hz, which was ~30–40 dB more sensitive than that measured in larval coral reef fishes (e.g., damselfishes) that lack swim bladder horns. C. ocellatus did not show any ontogenetic changes in sensitivity to sound pressure, which may be explained by the fact that the growth of the swim bladder horns maintains the small distance between the swim bladder and ear that was established earlier during the larval stage. The timing of the development of the swim bladder horns suggests that if the laterophysic connection has a sensory acoustic function, its presence in individuals >29 mm SL suggests that its role is limited to post-settlement, reef-based behaviors.

A new connection: Enhanced hearing ability in the New Zealand bigeye, Pempheris adspersa.

Recently the bigeye, Pempheris adspersa, has been found to be one of the few sound producing fish found in the temperate marine waters of New Zealand. An initial crude morphological examination of this species found a special connection, analogous to that of the well-defined laterophysic connection, between the otic capsule and the lateral line recess. The aim of the present study was to characterize the hearing ability of the bigeye using auditory evoked potentials, understand the role of this special connection, and describe the morphology of the hearing structures using microCT and MRI techniques. The novel connection consists of a robust ligament directly connecting the otic capsule to the lateral recess, with the swim bladder running directly posterior to the ligament. Pempheris adspersa could hear in the frequency range 100–1000 Hz, with greatest sensitivity between 100–800 Hz. Cutting the connecting ligament resulted in a 15–20 dB threshold shift, with a further 5–10 dB shift after swim bladder puncture. This connection represents a completely novel hearing specialization and shows that the lateral line is directly connected to the otic capsule, enhancing the hearing ability of this species especially at low frequencies (100–200 Hz).

Sound production and hearing in coral reef butterflyfishes.

Butterflyfishes (family Chaetodontidae) exhibit a diversity of close affiliative social behaviors. All 87 species of Chaetodon have a laterophysic connection and extensions of the anterior horns of the swim bladder near the otic capsule, which are proposed to impart sound pressure sensitivity to the normally mechanosensitive lateral line and acceleration‐sensitive inner ear. Video kinematic analyses reveal that the motor action patterns used to produce pulsed sounds vary among species. The sound production mechanisms in Chaetodon and Forcipiger do not appear to be conserved, thus sound production may have evolved independently within the family. Species with long swim bladder horns have lower AEP hearing thresholds than those without, and deflation of the horns and bladder decreases hearing sensitivity in the former group. When the laterophysic connection and swim bladder horns are physically disrupted in wild fish, movement within their territories decreases and fish pairs swim closer together. Thus, the low intensity sounds produced by butterflyfishes may favor close social behaviors that increase communication efficiency among individuals on a noisy coral reef. We are currently investigating how hydrodynamic flow fields produced during social interactions may be used for intraspecific communication during these natural behaviors.

Acoustic communication in territorial butterflyfish: test of the sound production hypothesis

Butterflyfishes are conspicuous members of coral reefs and well known for their visual displays during social interactions. Members of the genus Chaetodon have a unique peripheral arrangement of the anterior swim bladder that connects with the lateral line (the laterophysic connection) and in many species projects towards the inner ear. This morphology has lead to the proposal that the laterophysic connection and swim bladder system may be a specialized structure for the detection of sound. However, the relevant stimuli, receiver mechanisms and functions for these putative hearing structures were unknown because butterflyfishes were previously not recognized to produce sounds during natural behavior. We performed field experiments to test the hypothesis that Chaetodon produces sounds in natural social contexts. Acoustic and motor behaviors of the monogamous multiband butterflyfish, C. multicinctus, were evoked and recorded by placement of bottled fish into feeding territories of conspecific pairs. We demonstrate that territory defense includes the production of agonistic sounds and hydrodynamic stimuli that are associated with tail slap, jump, pelvic fin flick and dorsal-anal fin erection behaviors. In addition, grunt pulse trains were produced by bottled intruders and are tentatively interpreted to function as an alert call among pair mates. Acoustic behaviors include low frequency hydrodynamic pulses <100 Hz, sounds with peak energy from 100 Hz to 500 Hz, and a broadband high frequency click (peak frequency=3.6 kHz), which is produced only during the tail slap behavior. These results provide a biological framework for future studies to interpret the proximate function of the acoustico-lateralis sensory system, the evolution of the laterophysic mechanism and their relevance to butterflyfish social behavior.

Sound communication by the forceps fish, Forcipiger flavissimus (Chaetodontidae)

The forceps fish, Forcipiger flavissimus (family Chaetodontidae), lacks the anterior swim bladder horns and laterophysic connection that are proposed to improve processing of acoustic signals in the genus Chaetodon. Despite the lack of hearing specializations, laboratory experiments using hydrophones synchronized to video revealed the forceps fish produce at least three sounds: (1) a pulse (21‐ms duration, peak frequency=318 Hz) associated with rapid cranial elevation, (2) a low‐frequency pulse (9‐ms duration, peak frequency=41 Hz) associated with anal fin retraction and elevation, and (3) a high‐frequency broadband click (3‐ms duration, peak frequency=7924 Hz) associated with tail slap behavior. Auditory evoked potential experiments demonstrate that hearing thresholds for this species are 10–21 dB higher than Chaetodon in the 200–600‐Hz band. High‐speed kinematic analyses show that motor movements associated with some acoustic behaviors are different than those in Chaetodon, thus the presence of sound production may be the ancestral state for the family but the mechanisms are divergent. Field observations on Hawaiian reefs reveal that forceps fish occur in pairs and trios that may be haremic, and use acoustic communication among group members.[Work supported by NSF IBN0137883 to TT.]

The physoclistous swim bladder of chaetodontid butterflyfishes: Implications for acoustic function

Butterflyfishes (genus Chaetodon) have a swim bladder lateral line connection (laterophysic connection, LC), hypothesized to convert sound-induced oscillations of the swim bladder into fluid flow in the lateral line system and/or ear. Evaluation of LC function is dependent upon an understanding of swim bladder acoustics, which is a function of swim bladder anatomy. We used several anatomical methods (including CT) to describe swim bladder and tunica externa and tunica interna morphology (including gas gland/rete mirabile complex and the oval, responsible for gas secretion and resorption) in Chaetodon and Forcipiger. Swim bladder and tunica externa morphology differ between Chaetodon spp. with different LCs morphologies. A perforated transverse diaphragm divides the gas volume into two compartments. The gas gland/rete mirabile complex is in the ventral midline of the anterior compartment; it varies in morphology and is largest in species with a direct LC. The oval, defined by an extensive capillary network, occupies the entire tunica interna of the posterior compartment, so that diaphragm position determines oval size. These data raise questions about swim bladder structure-function relationships with respect to the reception and transduction of acoustic stimuli in coral reef fishes. [Work supported by NSF Grant IBN-0132607 to J.F.W.]

Acoustico‐lateralis communication in coral reef butterflyfishes

Butterflyfishes are conspicuous members of coral reefs and well known for their pairing behavior and visual displays during social interactions. Members of the genus Chaetodon have a unique arrangement of the anterior swim bladder horns that connect with the lateral line (the laterophysic connection) and also project towards the inner ear, but functions for this putative acoustico‐lateralis adaptation were not known. Field experiments demonstrate that the monogamous multiband butterflyfish, C. multicinctus, produces hydrodynamic pulses and sounds during territorial defense, and pulse trains that may be an alert call to the mate. In field choice tests, individuals could distinguish mates from nonmates and produced different calls to each, thus demonstrating the existence of mate recognition and context‐specific sound production. Laboratory experiments show that sound production differs among sexes, hydrodynamic pulses are of low frequency (<100 Hz), and sounds have peak energy from 100–500 Hz. Auditory evo...

The laterophysic connection and swim bladder of butterflyfishes in the genus Chaetodon (Perciformes: Chaetodontidae)

The laterophysic connection (LC) is an association between bilaterally paired, anterior swim bladder extensions (horns) and medial openings in the supracleithral lateral line canals that diagnoses butterflyfishes in the genus Chaetodon. It has been hypothesized that the LC makes the lateral line system sensitive to sound pressure stimuli that are transmitted by the swim bladder horns and converted to fluid flow into the lateral line system via a laterophysic tympanum. The purpose of this study was to define variation in the morphology of the LC, swim bladder and swim bladder horns among 41 Chaetodon species from all 11 Chaetodon subgenera and a species from each of four non-Chaetodon genera using gross dissection, histological analysis as well as 2D or 3D CT (computed tomographic) imaging of live, anesthetized fishes. Our results demonstrate that the lateral line system appears rather unspecialized with well-ossified narrow canals in all species examined. Two LC types (direct and indirect), defined by whether or not the paired anterior swim bladder horns are in direct contact with a medial opening in the supracleithral lateral line canal, are found among species examined. Two variants on a direct LC and four variants of an indirect LC are defined by combinations of soft tissue anatomy (horn length [long/short] and width [wide/narrow], number of swim bladder chambers [one/two], and presence/absence of mucoid connective tissue in the medial opening in the supracleithrum). The combination of features defining each LC variant is predicted to have functional consequences for the bioacoustics of the system. These findings are consistent with the recent discovery that Chaetodon produce sounds during social interactions. The data presented here provide the comparative morphological context for the functional analysis of this novel swim bladder-lateral line connection.

The evolution of the laterophysic connection with a revised phylogeny and taxonomy of butterflyfishes (Teleostei: Chaetodontidae)

The higher-level relationships of butterflyfishes were examined using 37 morphological characters. This analysis combines characters derived from a histological study describing variation in the morphology of the laterophysic connection (an association between the swim bladder and the lateral-line canals) with previously described morphological characters. The phylogenetic analysis resulted in four equally parsimonious trees that only differed in the placement of two of the 11 chaetodontid genera (Amphichaetodon and Forcipiger). We compare our analysis with previous hypotheses, present a new taxonomy consistent with the proposed cladistic relationships, and diagnose Chaetodon with five unreversed synapomorphies, including the evolution of characters composing the laterophysic connection. A new character-based diagnosis of Chaetodon is provided and species are allocated accordingly; Chaetodon now includes the former Parachaetodon ocellatus and excludes the former subgenera Prognathodes and Roa. The evolution of the laterophysic connection is examined by optimizing character-state transformations on the new hypothesis of relationships.

The evolution of the laterophysic connection with a revised phylogeny and taxonomy of butterflyfishes (Teleostei: Chaetodontidae)

AbstractThe higher‐level relationships of butterflyfishes were examined using 37 morphological characters. This analysis combines characters derived from a histological study describing variation in the morphology of the laterophysic connection (an association between the swim bladder and the lateral‐line canals) with previously described morphological characters. The phylogenetic analysis resulted in four equally parsimonious trees that only differed in the placement of two of the 11 chaetodontid genera (Amphichaetodon and Forcipiger). We compare our analysis with previous hypotheses, present a new taxonomy consistent with the proposed cladistic relationships, and diagnose Chaetodon with five unreversed synapomorphies, including the evolution of characters composing the laterophysic connection. A new character‐based diagnosis of Chaetodon is provided and species are allocated accordingly; Chaetodon now includes the former Parachaetodon ocellatus and excludes the former subgenera Prognathodes and Roa. The evolution of the laterophysic connection is examined by optimizing character‐state transformations on the new hypothesis of relationships.

The laterophysic connection: A novel specialization thought to enhance sound pressure sensitivity in butterflyfishes (Chaetodontidae, Chaetodon)

Morphological specializations that enhance sound reception have been described among fishes, but sources of behaviorally-significant sound stimuli and sound transduction mechanisms are known for very few bony fishes. Butterflyfishes in the genus Chaetodon have a unique sensory specialization, the laterophysic connection (LC), defined anterior swim bladder extensions (horns) in association with medial openings in the lateral line canals of the cranial supracleithral bones. The LC is hypothesized to enhance sensitivity of both the lateral line and ear to sound pressure. Variation in LC morphology among species is defined by variation in soft tissues and is thought to be functionally significant. Preliminary field studies demonstrate that C. multicinctus produces sounds during agonistic interactions, thus providing a source of potentially relevant sound stimuli. Presence of an inflated swim bladder in close proximity to well-developed supracleithral openings in pelagic tholichthys stage individuals (15 mm SL) and horn development at the end of the tholichthys stage (25–29 mm SL) in C. ocellatus suggests that sound may also play an important role in the early life history of Chaetodon. [Work supported by the NSF IBN-9603896 to J.F.W.]

The Temporal Region of the Cranium of Loricarioid Catfishes (Teleostei: Siluriformes): Morphological Diversity and Phylogenetic Significance

The morphology of the temporal region of the cranium of the monophyletic loricarioid catfishes was examined in representatives of the families Trichomycteridae, Callichthyidae, Scoloplacidae, Astroblepidae, and Loricariidae, and compared to non-loricarioid outgroup taxa. The results indicate the presence of derived specializations in the morphology of the pterotic bone, swimbladder capsule, lateral-line nerve, and associated structures which have not been previously recognized. Astroblepids, callichthyids, loricariids and scoloplacids differ from trichomycterids and non-loricarioid catfishes in having a reduced number of bones in the temporal region. Loricariids share with astroblepids and some trichomycterids the presence of direct contact between the trunk lateral-line canal and swimbladder capsule chamber; however, only loricariids have the lateral-line canal in direct contact with the swimbladder membrane, resulting in a laterophysic connection in addition to the otophysic connection between inner ear and swimbladder characteristic of otophysan fishes. Derived trichomycterids share with the outgroups Amphiliidae, Plotosidae and Sisoridae a cranial exit of the posterior lateral-line nerve separate from that of the vagus nerve, whereas both nerves exit the cranium via a common foramen in other loricarioids and outgroup catfishes. Callichthyids share with scoloplacids and loricariids a lateral-line nerve traversing the swimbladder capsule. Loricariids are further modified in having a compound pterotic bone that is double-layered and bears the postotic canal on the ventral layer. The dorsal layer is posteriorly expanded to enclose the lateral opening of the swimbladder capsule and an expanded capsule chamber. Based on the previously well-established scheme of interrelationships among loricarioid families, we infer that much of the variation in temporal cranial morphology over the course of loricarioid evolution has involved independent convergence toward increased functional association of primitively separate sensory structures of the octavolateralis system.

The laterophysic connection in chaetodontid butterflyfish: morphological variation and speculations on sensory function.

The laterophysic connection is a novel specialization in chaetodontid butterflyfish, in which paired diverticula of the swim-bladder ('horns') extend anteriorly and approach or directly contact a medial fossa in the lateral line canal contained within the supracleithrum. This study examined the morphology of the laterophysic connection in eight ecologically diverse species belonging to five subgenera within Chaetodon. Two types of laterophysic connections, indirect and direct, were found among Chaetodon species. Intraspecific variation (including sexual dimorphism) in the morphology of the laterophysic connection was not found. The type of laterophysic connection is not correlated with ecological characteristics among Chaetodon species, but appears to be correlated with subgeneric affinities of Chaetodon species. The presence of swim-bladder horns probably increases pressure sensitivity to the inner ear. It is suggested that the presence of a direct laterophysic connection, and possibly an indirect laterophysic connection, imparts pressure sensitivity to the lateral line canal system as well.

Laterophysic Connection: A Unique Link between the Swimbladder and the Lateral Line System in Chaetodon (Perciformes: Chaetodontidae)

The auditory and lateral line systems of teleost fishes are complementary in their ability to detect mechanical stimuli in water (Kalmijn, 1988, 1989; Coombs, 1994). The lateral line system is normally sensitive only to local incompressible flow fields arising from predators, prey, neighbors in a school, and environmental obstacles (reviewed by Montgomery et al., 1995). In contrast, the otolithic organs of the inner ear respond to whole-body accelerations generated by the same local flow fields to which the lateral line system responds. Enhanced sensitivity of the inner ear to propagated pressure waves (sound) is a specialized function of the inner ear of teleost fishes (Kalmijn, 1989), which is the result of the presence of a volume of compressible fluid (i.e., the swimbladder) in the vicinity of the inner ear. Morphological specializations in which the swimbladder is brought into close or direct contact with the inner ear are generally known as otophysic connections and occur in some or all species in all four lineages of teleost fishes (Osteoglossomorpha, Elopomorpha, Clupeomorpha, Euteleostei, reviewed by Schellart and Popper, 1992). It seems reasonable that the lateral line system could also be made pressure sensitive by placing an air cavity in the vicinity of, or in direct contact with, a lateral line canal. There are only two known examples of this type of sensory specialization: the recessus lateralis of clupeomorph fishes; and the unique connection between the inner ear and the lateral line