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  • Final Report Summary - EVOMORPHASIS (Evolutionary morphology of accessory auditory structures in piranhas, pacus, and related serrasalmid fishes: is acute hearing an adaptation for prey location?)

Final Report Summary - EVOMORPHASIS (Evolutionary morphology of accessory auditory structures in piranhas, pacus, and related serrasalmid fishes: is acute hearing an adaptation for prey location?)

PROJECT WEBSITE AND CONTACT DETAILS

http://www.kellyboyle.info/evomorphasis.html

Kelly S. Boyle kboyle@hawaii.edu
Anthony Herrel, MNHN, CNRS, anthony.herrel@mnhn.fr

WORK CARRIED OUT TO ACHIEVE PROJECT OBJECTIVES

Objective 1: Morphological Variation and Innovation of Serrasalmid Fishes

In order to examine morphological variation of peripheral auditory anatomy in serrasalmid fishes, microCT scans were performed on 54 specimens belonging to 20 species and 13 genera. Segmentation of bones and soft tissues was completed with Avizo 7.0 software in order to produce 3D reconstructions of the following bones and features (Fig. 1, see attachment): vertebrae 1-4, Weberian ossicles, bones associated with the Weberian morphology (claustrum, os suspensorium, neural complex), the neurocranium, otoliths, and the swim bladder (anterior and posterior chambers). Volumes of structures (mm3) were determined in Avizo.
In order to characterize size-free shape variation of structures among individuals and species, 3D-geometric morphometrics was performed using a combination of homologous landmarks, sliding curve landmarks, and sliding surface landmarks was used. Sliding surface landmarks were initially projected from a target specimen and iteratively slid relative to the template until convergence of minimal bending energy and then iteratively slid to minimize the bending energy relative to the Procrustes consensus of the entire dataset until convergence. Species averages were determined from the Procrustes consensus of individual specimens. Principal components analyses (PCA) were used to determine the main axes of landmark variation among the species dataset for different structures and Canonical Variates Analyses (CVA) were used to determine the morphological features among landmarks that best separate broad ecological groups (Fig. 2, see attachment) based on the feeding habits and habitat associations of different species reported from the literature: fish eating carnivores, fruit and seed eating species, and aquatic plant feeding species that occur among river rapids. These analyses have been completed for the scaphium, intercalarium, tripus, vertebra 2 (v2), and the lagenar otolith. Additional reconstructed data exists for the neurocranium, claustrum, vertebrae (1, 3, and 4), and neural complex for these fishes and shape analyses of these structures are on going.

Objective 2: Hearing Ability And Associated Morphology Of Various Serrasalmid Fishes

We have collaborated with researchers at the University of Liège (Dr. Eric Parmentier and Geoffrey Melotte) who are studying fish hearing with auditory evoked potentials. We have reconstructed the morphology of the otoliths, neurocranium, Weberian ossicles, anterior vertebrae, neural complex, and swim bladders of five species that were tested for audition: Piaractus brachypomus, Myleus schomburgkii, Metynnis lippincottianus, Serrasalmus elongatus, and Pygocentrus nattereri. These data will be used to determine if particular Weberian ossicle, otolith, and swim bladder shapes and sizes are associated with differences in auditory sensitivities at specific sound frequencies. These five species are from the three main clades of the serrasalmid phylogeny and include carnivorous and herbivorous species.

Obective 3: Prey Location Behavior And Sound For Serraslmid Fishes

In order to test what auditory cues may be associated with feeding in serrsalmid fishes, and to determine how fish behaviorally respond to the presence of such sounds, we performed behavioral trials with fish in aquaria. We performed experiments at the Laboratory of Functional and Evolutionary Morphology at the University of Liège (Ulg) and at the Antwerp Zoo. We recorded sound while fish were fed in small aquaria <500L (Ulg) and large aquaria >10000 (Antwerp). Audio recordings included splash sounds from food falling over the surface, a mimic of cues that occur for serrasamid fishes of inundated South American forests that feed on seeds and fruits that fall into rivers. In addition, we recorded sounds of aggressive feeding interactions (splashing and swimming piranhas) and mastication of different foods (mussels, fish, prepared foods, and nuts) (Fig. 3, see attachment). Species tested included Pygocentrus nattereri, Pygopristis denticulata, Metynnis lippincottianus, Myleus rubripinnis, Piaractus brachypomus, and Colossoma macropomum.
We conducted acoustic playback experiments in order to determine if sounds associated with serrasalmid feeding affect fish behavior. Feeding and splash sounds were played back via underwater speaker. Sequences of sound stimuli were played back for short durations <20s followed by several minute intervals over periods of about 25 minute. A video camera was used to examine movements of fish in aquaria in order to determine if sounds elicit searching behavior, if fish orient towards sounds, and if sounds are attractive.

MAIN RESULTS

Morphological Variation And Innovation

This is the first detailed, comprehensive study of Weberian apparatus shape and size among a single family otophysan fishes. The study has examined intra and interspecific variation in the family. Analyses thus far indicate a significant phylogenetic signal of shape, as revealed by the relative positions of landmarks for all bones tested thus far, but not for the lagenar otolith. CVA analyses revealed that for all morphologies analyzed thus far, that taxa that feed on submerged aquatic plants in rapids (rheophilic) have distinctive morphologies from the other ecological groups. Further, these differences are not explained simply by phylogenetic history alone. Rheophilic species are likely to live in environments with higher background noise from water flow. Similar environments have higher particle velocity noise levels across frequencies within the range of teleost fish hearing and higher noise pressure levels across mid-range frequencies within fish hearing. Rheophilic serrasalmids in this study had a less ornamented lagenar otolith with a shorter antirostrum and pseudoantirostrum. These features, along with smaller lagenar bullae may be potential adaptations for life in noisier environments. In addition, large differences were observed between the shape of v2 among ecological groups. This vertebra has large transverse processes that extend laterally and in some species anteriolateral. Rheophilic species have anterolateral shaped vertebrae that may have coevolved this morphology with the small lagenar bullae of the otic region of the skull that occurs in these species.

Prey Location Behavior

Splash sounds consisted of a low frequency component <100 Hz, a strong moderately high frequency 500-1000Hz, and a weaker broad band high frequency component from 1->5kHz. Intense feeding by shoals of piranhas also consists of low frequency components close to the source and high frequency components that propagate to greater distances. When fish masticate food, higher frequency components produce short broadband sounds that produce high frequency components. Low frequency components have the potential to stimulate the lateral line and the particle motion sensitive component of fish hearing: the lagena in otophysan fishes. Higher frequency components of ecological sounds, both near and at a distance from the source, and low frequency components at greater distances, will stimulate the sacculus via vibrations of the swim bladder transduced by the Weberian ossicles.
Preliminary results from sound playbacks at the Antwerp Zoo indicate that fish may be responding to sound. In Antwerp, mature fish appear to have responded to some acoustic cues. Qualitatively fish appeared to increase swimming activity and in some cases orient towards sounds during playbacks. A detailed analysis, tracking movements of individual fish before, during, and after stimuli to see if fish changed the orientation and increased swimming activity during and immediately after stimuli is currently underway.

CONCLUSIONS

Results from this study have shown that substantial variation exists in the peripheral auditory morphology between species within a single family. Analyses indicate that some shape features are associated with feeding ecology, while other features appear to show phylogenetic trends without a clear ecological pattern. These results suggest that some features are associated with certain acoustic ecologies, while others may be related to other evolutionary trends in the family, or may have no functional consequences. These findings on the morphology of Weberian apparatus features will form the basis of hypotheses on how certain shapes and size trends of these features are associated with different auditory capacities. Both frugivorous – granivore species and predatory species appear to possess more developed lagenar bullae and otoliths, as well as more rounded scaphium, a more robust intercalarium-verterbral articulation, and a less elaborated anterior process of the tripus than rheophilic species that occur in rapids. Large lagenar bullae and ornamented otoliths may provide increased sensitivity to sound particle motion, as the lagena plays a role in particle motion sensitive hearing in otophysan fishes. Differences in Weberian ossicles between rheophilic species and other serrasalmids indicates that there may be different adaptive requirements for sound pressure transduction in noisy and quiet freshwater environments. Hearing sensitivities from five species will soon be incorporated into the analysis and will provide an opportunity to determine how differences in Weberian ossicle shape and size affect sensitivity at specific frequencies.
Behavioral experiments demonstrated that acoustic cues associated with serrasalmid feeding include both low frequency components that may be especially relevant at close range to sound sources, as well has higher frequency components that may be important cues at greater distances from sources. Initial results indicate that fish may be aroused by acoustic cues associated with their feeding ecology. Both frugivore-granivores and predatory piranhas may encounter broadband/high frequency sounds associated with food. Frugivore-granivore species may be aroused by splash sounds associated with falling fruits and seeds, which may stimulate the fish to initiate searching behaviors incorporating other modalities such as vision. Piranhas, which are known to move towards disturbances such as swimming shoals of fish and splashing, commotion that could be associated with group predation events, may respond to such splash sounds by increasing there swimming in a search pattern.

POTENTIAL IMPACT OF THE PROJECT

This study will increase the understanding of how the environment has influenced the evolution of accessory hearing structures in fishes and will inspire future studies on peripheral auditory morphology related to hearing sensitivity and ecology. This is the first study we are aware of to use a geometric morphometric approach to examine shape variation of the auditory periphery in fishes and we expect that this may encourage further study in other otophysan fishes in order to examine other evolutionary and functional trends associated with these features.

Related information

Reported by

MUSEUM NATIONAL D'HISTOIRE NATURELLE
France
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