Intraspecific variability of the saccular and utricular otoliths of the hatchetfish Argyropelecus hemigymnus (Cocco, 1829) from the Strait of Messina (Central Mediterranean Sea)

PLOS ONE RESEARCH ARTICLE Intraspecific variability of the saccular and utricular otoliths of the hatchetfish Argyropelecus hemigymnus (Cocco, 1829) from the Strait of Messina (Central Mediterranean Sea) a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 Claudio D’Iglio ID1, Sergio Famulari ID1, Marco Albano ID1, Alex Carnevale1, Dario Di Fresco1, Mariachiara Costanzo1, Giovanni Lanteri1, Nunziacarla Spanò2, Serena Savoca ID2☯*, Gioele Capillo ID3☯ 1 Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Messina, Italy, 2 Department of Biomedical, Dental and Morphological and Functional Imaging, University of Messina, Messina, Italy, 3 Department of Veterinary Sciences, University of Messina, Messina, Italy ☯ These authors contributed equally to this work. * OPEN ACCESS Citation: D’Iglio C, Famulari S, Albano M, Carnevale A, Di Fresco D, Costanzo M, et al. (2023) Intraspecific variability of the saccular and utricular otoliths of the hatchetfish Argyropelecus hemigymnus (Cocco, 1829) from the Strait of Messina (Central Mediterranean Sea). PLoS ONE 18(2): e0281621. https://doi.org/10.1371/journal. pone.0281621 Editor: Sanja Puljas, University of Split, Faculty of science, CROATIA Received: October 7, 2022 Accepted: January 27, 2023 Published: February 14, 2023 Copyright: © 2023 D’Iglio et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Abstract Mesopelagic species are enjoining increasing attention due to the growing impact of fisheries activities on deep marine biocenosis. Improving the knowledge base on mesopelagic species is required to enhance their conservation due to the knowledge gaps regarding many species and families. In this context, otoliths can be fundamental to assessing their life history, ecomorphological adaptation to the deep environment and stock composition. The present paper aims to explore the saccular and utricular otoliths morphology and intraspecific variability of the hatchetfish, Argyropelecus hemigymnus, from the Strait of Messina. Lapilli and sagittae were collected from 70 specimens and separated into four size classes. Morphometric, shape and SEM investigations were performed to describe their morphology, contours, and external structural organization, also studying their intraspecific variability related to sample sizes and differences between otolith pairs. Results showed an otolith morphology different from those reported in the literature with fluctuating asymmetry in sagittae and lapilli belonging to Class IV, and a high otolith variability between all the size classes. Data herein described confirm the otoliths singularity of the population from the Strait of Messina, shaped by a unique marine environment for oceanographic and ecological features. Data Availability Statement: All relevant data are within the paper and its Supporting information files. Funding: The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Introduction The vertebrates’ inner ear represents a highly specialized organ for sound detection, motion/ position measuring, and equilibrium regulation [1, 2]. All the vertebrates (except for the jawless) share a similar inner ear morphology, with one ear for side, each characterized by three PLOS ONE | https://doi.org/10.1371/journal.pone.0281621 February 14, 2023 1 / 31 PLOS ONE Investigation on Argyropelecus hemigymnus (Cocco, 1829) saccular and utricular otoliths semicircular canals. In most non-mammalian vertebrates, these canals present three otolithic end organs (utricle, saccule, lagena). Within each of these are calcium carbonate crystals that in teleost fishes solidify in single acellular masses, called otoliths (respectively lapillus, sagitta, asteriscus) [3]. These are characterized by continued growing during the entire fish’s lifetime, with a daily deposition of new material [4, 5]. Their isolation from the external environment and their capability to be metabolically inert make them an essential tool for fish life history studies [4, 6]. Especially sagittae (the largest among otoliths in non-otophysan species [7]) have been extensively used in many research fields (e.g., fisheries science [8–12], ecology [13– 20], taxonomy [21–25], palaeontology [26–28] and eco-geochemistry [29]) due to their species-specific morphology [25, 30, 31], their persistence in ancient sediments [32] and stomach contents of ichthyophages predators [13–16], and their inter-specific variability in morphology, microstructure and microchemical composition [33, 34]. Despite lapilli and asterisci being widely described in many species [35–37], there is relatively less information, if compared with sagittae, regarding their morphology and diversity, especially in marine teleost [38]. Lapilli has been broadly used for the identification of otophysan fishes (being larger than sagittae) [39, 40], but due to their generally small size, their low persistence in geological layers and predators’ stomach contents, and their almost completely unknown intra and interspecific diversity, the knowledge base on these otoliths is still limited, especially regarding Mediterranean bony fishes. The Mediterranean Sea is a semi-enclosed basin characterized by enhanced biodiversity and a high anthropogenic impact related to pollution, fisheries activities, and urbanization. The growing impact of human activities (especially fisheries [41–44]) on Mediterranean deep environments has led the scientific community to focus on meso- and bathypelagic communities. Due to their vertical migrations and trophic relationships, these play a fundamental ecological role in the energy flowing and carbon transport between different marine domains [45– 54]. Mesopelagic fishes show a great abundance in biomass, being the main component of the deep scattering layer (DSL) and mesopelagic zone, and the most abundant vertebrates on earth for their density and diffusion in all the Oceans [55, 56]. Several studies have been focused worldwide on these species’ distribution, biology, biodiversity and ecology [51, 56–59], also investigating morphology, microstructures and growth of sagittae [57, 60–65]. Despite this, the knowledge base on mesopelagic fishes remains scarce, with several gaps regarding the biology and eco morphology of many species and families. Due to their deep distribution, these teleosts are mainly sampled with expensive methods, such as trawling (being large specimens abundant in trawling discards and by-catch) or other nets for micronekton sampling (e.g., Isaacs-Kidd Midwater Trawl Net, Environmental Sensing System, young fish trawl) [58, 66]. However, the s (...truncated)