Vertebrate ear is the organ responsible of the sense of hearing and balance, with a high structure and functioning variability inside the group. The semicircular canals of the vestibular part of the inner ears are the structures allowing to the detection of angular acceleration, while the detection and production of sounds is regulated by several structures. In the entire group, the transduction mechanisms for the conversion of sounds (and vestibular stimuli) involves the sensory hair cells, with their cilia, that, once bent due to the pressure component of particle movements related to sound, induce a physiological response of cells. This stimulates the innervating eighth cranial nerve, by the conversions of head movements and sounds into neurochemical signal. Concerning teleost species, their inner ear is characterized by the presence of three semicircular canals, with their end organs (ampullae) and sensory cristae, and three otolith end organs. These form three pouches (utricle, saccule, lagena), and their rostro-caudal angular orientation (taxon specific) is essential for sound- source location. Otoliths are located inside the otolithic end organs (one for each end organs): sagitta in sacculus, lapillus in utricle and asteriscus in lagena. These thanks to their strictly connection with the sensory epithelium (macula), can convert the particle motion related to sound field in physiologically response resulting in nerve stimulation. Fishes using only the direct stimulation to detect sound (called “hearing generalists”) show a lower sensitivity and a narrower band width of hearing, while the so called “hearing specialists” can detect sound with indirect pathways (through the detection of sound pressure) thanks to accessory auditory structures, peripheral to the ear. Otoliths are solid carbonate acellular masses (with a small fraction of proteins), biomineralizing during the entire teleost’s life with a daily growth with a metabolic inertia. Any chemical compounds or elements added during the growth process is permanently maintained and, due to the continue growing during the entire animals’ lifecycles, otoliths can be the “flight recorder” of fishes. They can preserve several information on environmental conditions experienced by fishes, their life habits, metabolism, and physiology. For this reason, they are widely used to investigate migration pathways and pollution exposure, to validate age and identify stocks, being also used as metabolic indicators, natural tag, and mass marking. Among the interesting features of fish ears, the most striking is for sure the inter specific diversity, ranging from their gross structure to the sensory hair cells’ organization. Ear shape can be related both to fishes’ size and ear function, but it is almost unknown its significance. Concerning the most studied among otoliths, sagittae, they are often the most involved in hearing process, as reported for “hearing specialist” species. The morphological diversity of sagittae also involves the sensory epithelia (e.g., shape, size) and its relationship with otolith (e.g., coverage ratio of otolith on epithelia), with inter specific variation also in sulcus depth. The significance of this high variability at intra and inter specific level is almost completely unknown, but morphology directly influences otoliths’ functioning. The peculiar chemistry of otoliths, their growing and deposition dynamics, their intra and inter specific variability in morphology and shape, all these features make otoliths essential tools used, from more than a century, to investigate many aspects of teleost’s lifestyle, taxonomy, and population dynamics, as well as to obtain essential information for fisheries management and conservation purposes. Understand the relation between habitats, ecological conditions and otoliths is essential to clarify the dynamics allowing their intra and inter specific diversity, deepening the knowledge on the development dynamics of the entire inner ear, and its relationships with environmental features and different habitat’s preferences. This thesis aims to explore the information that otoliths can provide about the eco-morphological adaptation of Mediterranean teleost fishes to different environments, through the investigation of the intra and inter specific differences of several species characterized by different life habits and exploited habitats. Six cases of study have been provided, obtaining data on the variability of sagittae at intra and inter specific level, with useful information on the functional morphology of otoliths in the studied species. The intra specific variability of sagittae, in shape, morphology and external textural organization, has been analyzed at inter and intra population level, between different size classes, while the variability at inter specific level has been explored among species belonging to the same genus or family. Moreover, in two of the studied species, for the first time in the Mediterranean Sea, in addition to sagittae, they have been analyzed also lapilli and asterisci, providing a complete description to fill the gap about their intra specific variability. The first, the second and the third cases of study involved respectively the species belonging to Pagellus genus (P. erythrinus, P. bogaraveo, P. acarne), Mugilidae family (C. auratus, C. labrosus, O. labeo) and Macrouridae family (H. italicus, N. sclerorhynchus, N. aequalis, C. guentheri, C caelorhincus), exploring the inter and intra specific variability of sagittae in phylogenetically close species. The fourth and the fifth cases of study involved A. hemigymnus and B. belone, respectively, with the analysis of the three otoliths’ pairs (sagittae and lapilli of A. hemigymnus, sagittae, lapilli and asterisci of B. belone) at intra specific level to assess their variability in these deeply different species. The inter population variability of sagittae has been analyzed in the sixth case of study, involving S. porcus specimens, comparing the sagittae features of two populations inhabiting completely different environments. They have been also analyzed feeding habits, growth dynamics and age structures, comparing them with literature data from other geographical areas, to find a most clear correlation between environmental conditions and sagittae features. The results provided by the six cases of study have explored the diversity in morphology, mean shape, and morphometry of several Mediterranean teleost species, characterized by different life habits, habitat preferences and phylogenetic relationships. They were also described the inter and intra specific variability occurring between and within the different species, also providing, for the first time, data on the mean sagittae shape from shape analysis for many of them. Moreover, for the first time in the Mediterranean Sea, it was provided an accurate description, with data from shape, morphometric analyses, and their intra specific variability, of lapilli and asterisci belonging to A. hemigymnus and B. belone specimens. It was also confirmed the reliability for populations discrimination of sagittae in S. porcus, with the inter population analysis which provided several evidence on the high plasticity in sagittal otoliths features, feeding habits and somatic growth rates under different environmental pressures, experienced by specimens from two totally different habitats. All these data have opened new scenarios for future studies on the eco-morphology of the three otolith pairs from marine teleost species, to better understand the inner ear functioning and detect the mechanisms of population differentiation and speciation processes. Thanks to otoliths, and future advances in otoliths science, it will be possible to understand several aspects of species ecology, difficult to explore directly, and evolution. This will increase our knowledge about the ecological relationships and niche partitioning in marine communities, the dynamics of populations discrimination and the connection between phylogenetic and morphological differentiations.

THE ECOMORPHOLOGICAL ADAPTATION OF MARINE TELEOST FISHES REVEALED BY OTOLITHS

D'IGLIO, Claudio
2023-12-11

Abstract

Vertebrate ear is the organ responsible of the sense of hearing and balance, with a high structure and functioning variability inside the group. The semicircular canals of the vestibular part of the inner ears are the structures allowing to the detection of angular acceleration, while the detection and production of sounds is regulated by several structures. In the entire group, the transduction mechanisms for the conversion of sounds (and vestibular stimuli) involves the sensory hair cells, with their cilia, that, once bent due to the pressure component of particle movements related to sound, induce a physiological response of cells. This stimulates the innervating eighth cranial nerve, by the conversions of head movements and sounds into neurochemical signal. Concerning teleost species, their inner ear is characterized by the presence of three semicircular canals, with their end organs (ampullae) and sensory cristae, and three otolith end organs. These form three pouches (utricle, saccule, lagena), and their rostro-caudal angular orientation (taxon specific) is essential for sound- source location. Otoliths are located inside the otolithic end organs (one for each end organs): sagitta in sacculus, lapillus in utricle and asteriscus in lagena. These thanks to their strictly connection with the sensory epithelium (macula), can convert the particle motion related to sound field in physiologically response resulting in nerve stimulation. Fishes using only the direct stimulation to detect sound (called “hearing generalists”) show a lower sensitivity and a narrower band width of hearing, while the so called “hearing specialists” can detect sound with indirect pathways (through the detection of sound pressure) thanks to accessory auditory structures, peripheral to the ear. Otoliths are solid carbonate acellular masses (with a small fraction of proteins), biomineralizing during the entire teleost’s life with a daily growth with a metabolic inertia. Any chemical compounds or elements added during the growth process is permanently maintained and, due to the continue growing during the entire animals’ lifecycles, otoliths can be the “flight recorder” of fishes. They can preserve several information on environmental conditions experienced by fishes, their life habits, metabolism, and physiology. For this reason, they are widely used to investigate migration pathways and pollution exposure, to validate age and identify stocks, being also used as metabolic indicators, natural tag, and mass marking. Among the interesting features of fish ears, the most striking is for sure the inter specific diversity, ranging from their gross structure to the sensory hair cells’ organization. Ear shape can be related both to fishes’ size and ear function, but it is almost unknown its significance. Concerning the most studied among otoliths, sagittae, they are often the most involved in hearing process, as reported for “hearing specialist” species. The morphological diversity of sagittae also involves the sensory epithelia (e.g., shape, size) and its relationship with otolith (e.g., coverage ratio of otolith on epithelia), with inter specific variation also in sulcus depth. The significance of this high variability at intra and inter specific level is almost completely unknown, but morphology directly influences otoliths’ functioning. The peculiar chemistry of otoliths, their growing and deposition dynamics, their intra and inter specific variability in morphology and shape, all these features make otoliths essential tools used, from more than a century, to investigate many aspects of teleost’s lifestyle, taxonomy, and population dynamics, as well as to obtain essential information for fisheries management and conservation purposes. Understand the relation between habitats, ecological conditions and otoliths is essential to clarify the dynamics allowing their intra and inter specific diversity, deepening the knowledge on the development dynamics of the entire inner ear, and its relationships with environmental features and different habitat’s preferences. This thesis aims to explore the information that otoliths can provide about the eco-morphological adaptation of Mediterranean teleost fishes to different environments, through the investigation of the intra and inter specific differences of several species characterized by different life habits and exploited habitats. Six cases of study have been provided, obtaining data on the variability of sagittae at intra and inter specific level, with useful information on the functional morphology of otoliths in the studied species. The intra specific variability of sagittae, in shape, morphology and external textural organization, has been analyzed at inter and intra population level, between different size classes, while the variability at inter specific level has been explored among species belonging to the same genus or family. Moreover, in two of the studied species, for the first time in the Mediterranean Sea, in addition to sagittae, they have been analyzed also lapilli and asterisci, providing a complete description to fill the gap about their intra specific variability. The first, the second and the third cases of study involved respectively the species belonging to Pagellus genus (P. erythrinus, P. bogaraveo, P. acarne), Mugilidae family (C. auratus, C. labrosus, O. labeo) and Macrouridae family (H. italicus, N. sclerorhynchus, N. aequalis, C. guentheri, C caelorhincus), exploring the inter and intra specific variability of sagittae in phylogenetically close species. The fourth and the fifth cases of study involved A. hemigymnus and B. belone, respectively, with the analysis of the three otoliths’ pairs (sagittae and lapilli of A. hemigymnus, sagittae, lapilli and asterisci of B. belone) at intra specific level to assess their variability in these deeply different species. The inter population variability of sagittae has been analyzed in the sixth case of study, involving S. porcus specimens, comparing the sagittae features of two populations inhabiting completely different environments. They have been also analyzed feeding habits, growth dynamics and age structures, comparing them with literature data from other geographical areas, to find a most clear correlation between environmental conditions and sagittae features. The results provided by the six cases of study have explored the diversity in morphology, mean shape, and morphometry of several Mediterranean teleost species, characterized by different life habits, habitat preferences and phylogenetic relationships. They were also described the inter and intra specific variability occurring between and within the different species, also providing, for the first time, data on the mean sagittae shape from shape analysis for many of them. Moreover, for the first time in the Mediterranean Sea, it was provided an accurate description, with data from shape, morphometric analyses, and their intra specific variability, of lapilli and asterisci belonging to A. hemigymnus and B. belone specimens. It was also confirmed the reliability for populations discrimination of sagittae in S. porcus, with the inter population analysis which provided several evidence on the high plasticity in sagittal otoliths features, feeding habits and somatic growth rates under different environmental pressures, experienced by specimens from two totally different habitats. All these data have opened new scenarios for future studies on the eco-morphology of the three otolith pairs from marine teleost species, to better understand the inner ear functioning and detect the mechanisms of population differentiation and speciation processes. Thanks to otoliths, and future advances in otoliths science, it will be possible to understand several aspects of species ecology, difficult to explore directly, and evolution. This will increase our knowledge about the ecological relationships and niche partitioning in marine communities, the dynamics of populations discrimination and the connection between phylogenetic and morphological differentiations.
11-dic-2023
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