Description of Hyperostotic Bones Pattern in Hairtail Trichiurus lepturus

doi:10.21203/rs.3.rs-3419958/v1

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Description of Hyperostotic Bones Pattern in Hairtail Trichiurus lepturus

https://doi.org/10.21203/rs.3.rs-3419958/v1

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published 09 Jan, 2024

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Several studies have documented the occurrence of hyperostosis, a bone condition that results in bone thickening, in specimens of Trichiurus lepturus, an important commercial species. A total of 102 Hairtail fish samples from Rio de Janeiro, Brazil, were obtained from artisanal fishers and divided into four size classes. Biometric measurements and radiographic images were taken for all exemplars. Hyperostosis was observed in 69.69% of the individuals, with the first detection of the condition in an exemplar measuring from 385 mm in total length. The affected skeletal regions included the Cleithrum, Supraoccipital, Frontal, Dorsal Pterygiophores, and Hemal Spines. An increase in the occurrence frequency of hyperostosis was noticed in correlation with size, suggesting a connection with the aging process and an ontogenetic pattern for the species. Histological analysis indicated a high remodeling process in affected structures. Additionally, we highlight the species' daily vertical migration, associated with temperature variation, as a potential contributor to the onset of this osteological condition in marine teleosts.

Osteology

Hyperostosis

Trichiuridae

Bone development

Skeletal anomalies can impact the development of fish and may be a crucial factor for their survival in the wild (Jawad and Akyol 2018). However, not all anomalies result in the mortality of these individuals. The survival of certain organisms with bone deformities can be attributed to various factors, such as dietary habits and the absence of predators (Fjedall et al. 2021).

Hyperostosis is an osteological condition that results in a change in the mineralogical microstructure (Aguilera et al. 2017), leading to increased periosteal ossification and continuous remodeling of bone tissue (Gauldie and Czochanska 1990; Meunier et al. 2010; Olsen 1971; Smith-Vaniz et al. 1995; Aguilera et al. 2017), typically reported in acellular fish (Meunier et al. 1999, 2010). This condition can occur in a wide variety of bones, though certain regions are more commonly reported. Specifically, the cranial region, especially the supraoccipital crest, cleithrum, ribs, hemal and neural spines, as well as the dorsal and anal pterygiophores, seem to be more frequently affected (Desse et al. 1981; Smith-Vaniz et al. 1995; Tuna et al. 2023). However, other bones such as the premaxillae, maxillae, coracoids, rays, and spines of the dorsal fin, among others, also exhibit this condition (Murty 1967; Fierstine 1968; Smith-Vaniz et al. 1995; Al Albri et al. 2022).

The Trichiuridae family is characterized by fish with elongated bodies, with a tapered tail or a diminutive forked caudal fin. These fish are adaptable, thriving in a diverse range of habitats and depths (Nakamura and Parin 1993). Spanning a wide geographical distribution (Nelson et al. 2016; Froese and Pauly 2023), they are recognized as a vital fisheries resource in numerous regions (Hermida et al. 2020). The condition of hyperostosis is well-documented in the Trichiuridae family, impacting both current and ancient commercial fish species (James 1960; Olsen 1971; Al Nahdi et al 2016; Lima et al. 2002; Chanet 2018; Meunier et al. 2010). The genera Trichiurus Linnaeus, 1758 and Lepidotus Goüan, 1770 have been reported with instances of hyperostosis in species like Trichiurus lepturus Linnaeus, 1758, Lepidutos albyi (Sauvage, 1870), L. caudatus (Euphrasen, 1788), and L. proargenteus (a fossil record). James (1960) examined four distinct species from the Trichiuridae family found in Indian waters, but only identified the presence of hyperostosis in T. lepturus.

The hairtail Trichiurus lepturus is a circumglobal species distributed in tropical and temperate waters in the Atlantic, Pacific, and Indian Oceans, occurring all along the Brazilian coast (Menezes et al. 2003). They exhibit benthopelagic behavior, capable of moving several meters in the water column to feed presenting robust swimming capability (Zhang et al. 2016). They hold significant commercial importance worldwide, being a target species for various fishing fleets (Nakamura and Parin 1993; De la Cruz-Torres et al. 2014).

Several studies report the occurrence of hyperostosis in specimens of Hairfish with different frequencies of occurrence and affected skeletal regions. In bones located in the vertebral column area, James (1960) and Lima et al. (2002) found proportions in the quantities of hemal and neural spines that displayed the hyperostosis condition. Al Nahdi et al. (2016) compares different studies on the species regarding the occurrence of hyperostosis in neural and hemal spines for different locations. Lima et al. (2002) reports the fusion of sequential hyperostotic bones in specimens collected in Brazil.

While the reason for the development of hyperostosis remains unclear, some authors suggests the development of the condition to various factors, such as pathologies (Grabda 1982; Lima et al. 2002), adverse environment (Chang et al. 2008; Greenwood 1992; Schlüter and Kohring 2002), aid for swimming (Fierstine 1968; Paig-tran et al. 2016), aging (Aguilera et al. 2017; Gauldie and Czochanska 1990; Smith-Vaniz and Carpenter 2007), among others. Despite this, few studies demonstrated the development of the condition during the growth of these organisms. Tuna et al. (2023) showed the existence of an ontogenetic pattern of hyperostosis development, linking fish growth with the determination of the bone affected by the condition.

The aim of this study was to describe the ontogenetic pattern of hyperostotic bone development across different size classes in hairtail fish, a significant global commercial resource. This research will serve as a foundation for a better understanding of this condition that affects several marine teleost species.

2.1 Fish material

We analyzed 102 samples of Hairfish - Trichiurus lepturus (40 males, 43 females, and 19 of indeterminate sex) purchased from artisanal fishermen from two different estuaries – Guanabara Bay and Sepetiba Bay – in Rio de Janeiro, Brazil. Biometric measurements regarding total length (TL in mm) and weight (in grams) were taken. The specimens ranged from 184–1093 mm in TL and were categorized into four size classes (TL: < 300 mm; 300–600 mm; 600–900 mm, and > 900 mm).

2.2 Radiology

For radiological images, the specimens were thawed overnight and radiographed with the portable x-ray unit model Porta 100HF equipment (Job Corporation) at 0.6 meters from the animal, using the following settings of 60KV and 2.0 mAs. The dimensions of bones height and width were determined using the Image J software program (Bourne and Bourne, 2010).

2.3 Histology

The osteological samples were placed in EDTA for 72 h, subsequently washed in running water, dehydrated through a gradual sequence of absolute alcohol concentrations, bleached in xylene, and embedded in paraffin. Samples were cut into sections of 4-µm thickness by a rotary microtome, mounted on slides, and stained with Harris hematoxylin and eosin for analysis.

Hyperostosis was found in 69.60% of the specimens analyzed (Fig. 1), occurring in five different bones – Supraoccipital and Frontal (grouped under the Cranial - CR category); Cleithrum (CL); Dorsal fin Pterygiophores (PD) and Hemal Spines (HS).

No indication of hyperostosis was identified in specimens from the first size class (TL: < 300 mm – n = 17). The condition was first detected in a specimen measuring 385 mm, which displayed hyperostosis in three hemal spines. Individuals with a TL between 300–600 mm (n = 21) exhibited hyperostosis in the HS, CR and PD regions. From specimens measuring TL 600–900 mm (n = 43), hyperostosis manifested in all areas described for the species, occurring in high proportions - above 75% of individuals, except for the cleithrum. Individuals > 900 mm of TL (n = 21) presented high frequencies of hyperostosis in all four regions.

Multiple dorsal pterygiophores and hemal spines can be affected in the same individual (Fig. 2). The anterior section of the body has its dorsal pterygiophores affected sequentially. However, those structures do not exhibit a rounded aspect, in contrast to the typical appearance found in the hemal spines. In larger individuals, it's also possible to identify increased bone porosity – as demonstrated by the reduced density in the radiographic image. The number of affected PD was higher than HS, but the hyperostotic bone size was notable higher in HS (max: 42 mm in width). Although there are no fused bones, large hemal spines occupy the space of sequential hemal spines.

In the cranial bones, there was a notable thickening in both the supraoccipital crest and the frontal bone. However, not all individuals exhibited thickening in both bones, with the supraoccipital being much more prevalent than the frontal. The development pattern indicates a bottom-up movement as they grow (Fig. 3), suggesting that this thickening begins in the ventral portion and extends upwards in the cranial region.

The histological sections of the sample show significant new bone formation characterized by a prominent acellular bone matrix (newly formed bone), partially organized into lamellae, occasionally with the formation of spicules. The bone trabeculae are thick, interconnected, and present fissures (empty spaces). This results in the reduction of the interosseous spaces (which are irregular), characterizing the process of hyperostosis and active remodeling of the matrix.

Detecting hyperostosis isn't easily accomplished during routine inspections (Rapisarda et al. 2008; Giarratana et al. 2012). However, in some individuals, especially those with elongated and slender bodies like Trichiurus lepturus and Lepidotus caudatus, hyperostotic bones can be noticed by touch (James 1960; Grabda 1982; Lima et al. 2002). Giarratana et al. (2012) describe, in terms of commercialization, larger specimens with multiple bones affected tend to have a compromised fillet cut quality, affecting its aesthetic appearance. There's a possibility that hyperostosis can lead to bacterial contamination, loss of muscle tissue, imperfections, and the infeasibility of repeated cutting techniques. Lima et al. (2002) highlight the impracticality of automated filleting due to the presence of osteomas, as the machinery is designed for standard species. This necessitates an investment in both time and cost for manual processing (Branson and Turnbull 2008).

Species from tropical and subtropical shallow waters are more commonly reported to exhibit the hyperostosis condition than species from temperate waters (Smith-Vaniz et al. 1995). However, there are exceptions where temperate water species, such as Gadiformes (Smith-Vaniz et al. 1995), individuals of the oarfish Regalecus russellii Cuvier and Valenciennes, 1817 - a mesopelagic species from temperate waters (Paig-tran et al. 2016), or even freshwater species (Greenwood 1992), also show the condition. Paig-Tran et al. (2016) suggests that our perception of species with hyperostosis might reflect our more extensive knowledge of coastal species from tropical waters.

Numerous species were described by Smith-Vaniz et al. (1995) as having hyperostosis, and since then, new species have been reported from various locations (Al Albri et al 2022). Chanet (2018) analyzed the families exhibiting hyperostosis and found no apparent phylogenetic relationship, suggesting it might result from convergence. Due to hyperostosis displaying species-specific manifestations (Smith-Vaniz et al. 1995), some authors suggest hyperostosis as a potential criterion for the taxonomic identification of morphologically similar species (Yasuda and Mizuguchi 1969; Gauldie and Czochanska 1990; Smith-Vaniz et al. 1995; Guzman and Polaco 2002; Smith-Vaniz and Carpenter 2007; Rapisarda et al. 2008). Guzman and Polaco (2002) suggest that analyzing the patterns of hyperostosis could validate the existence of distinct species within the Trichiuridae family in both the Pacific and Atlantic Oceans.

Structures affected by the hyperostosis condition are typically associated with a species-specific pattern. However, taxonomically related species might display different regions affected by this condition (Smith-Vaniz et al. 1995). Commonly, the bones affected include neural and hemal spines, pterygiophores, ribs, and the supraoccipital (Desse et al. 1981). A single individual can develop multiple affected structures (Murty 1967; Tuna 2015). However, in the Trichiuridae family, there seems to be a higher occurrence of hyperostosis in the dorsal pterygiophores and hemal spines. Apart from these mentioned structures, only James (1960) reported the occurrence of hyperostosis in the supraoccipital of the T. lepturus.

The use of X-ray devices for the detection of skeletal changes and anomalies is extremely important, as it allows for high data reliability and increased processing speed, making it feasible to analyze a larger number of specimens. However, being a two-dimensional image, certain precautions regarding the detection of affected regions must be taken to correctly identify the occurrence of the hyperostosis condition in that particular bone. Potthoff et al. (1986) state that in adults of T. lepturus, the dorsal pterygiophores are accommodated between sequential intraneural spaces. This perception is crucial to determine whether hyperostosis is occurring in the neural spine or the dorsal pterygiophore.

Our data show an increase in the frequencies of occurrence in new regions as the individual grows and consequently ages, making it clear that there is an ontogenetic pattern in the development of hyperostosis in T. lepturus individuals. The increase in frequency of occurrence per bone region according to age demonstrates an aging process (Aguilera et al. 2017; Smith-Vaniz et al. 1995). The high frequencies found by Lima et al. (2002), Giarratana et al. (2012) and Al Nahdi et al. (2016) — with frequencies ranging from 94.5%, 80%, and 52.7%, respectively, contrast sharply with the lower values (9.6% and 16.5%) found by James (1960) and Gaevskaya and Kovaleva (1965). James (1960) reported a higher occurrence of hyperostosis in the hemal spines than in the neural spines of T. lepturus in Indian waters. Conversely, Lima et al. (2002) found for the same species in Brazilian waters, a greater proportion in neural spines than in hemal spines, although the hemal spines were described as fused. James (1960) also reports the fusion of bones containing hyperostosis, becoming a large bony mass.

One of the most markable characteristics of the presence of hyperostosis is the presence of highly vascularized bones with intense continuous bone remodeling (Smith-Vaniz et al. 1995), commonly reported with large vascular cavities (Meunier et al. 2010). The reasons for this differing process, as well as the causes behind the onset of the condition, remain unclear. The most evident difference appears to be the environment in which these organisms exist. Environmental factors such as water temperature and the presence of chemical elements in the water quality might be contributing to a higher frequency of the condition.

A wide variety of fish types, each with distinct habits, body structures, diets, and other variables, exhibit the hyperostosis condition. Paig-Tran et al. (2016) theorizes that one of the functions of hyperostosis might be that, from the size of maturation onwards, hyperostosis serves as a hardened focal point for stress concentration, providing support for locomotion or positioning, particularly in the oarfish – a fish with an exceedingly elongated body and a minimally mineralized skeleton. Fierstine (1968) describes how hyperostosis in the pterygiophores of species in the Caranx genus (Lacepède, 1801) might function as a broadening mechanism to keep the dorsal fin erect. Aguilera et al. (2017) state that the properties of muscles have their mechanical properties altered due to hyperostosis. Giarratana et al. (2012) found a positive correlation between the presence of hyperostosis in the pterygiophores of Lepidotus caudatus (Euphrasen, 1788), suggesting a mechanism for increasing body mass. Fjedall et al. (2021) found differences in the frequencies of hyperostosis between farmed and wild populations of Labrus bergylta Ascanius 1767, associating the development of the condition with repetitive swimming effort.

Among the various abiotic factors that govern the marine environment, temperature stands out as one of the most crucial. It has the ability to regulate species life stages (Liu and Cheng 2023). Temperature differences during the life cycle of species may be directly related to the development of the hyperostosis condition (Capasso 1997; Tuna et al. 2023). Aguilera et al. (2017) suggest that environmental stress can modify the microchemistry and homeostasis of the bone.

The Hairtail is an amphidromous species with a benthopelagic behavior that has a strong swimming ability, undertaking daily vertical migrations. During the day, the fish stay in deeper and colder waters, moving to shallower and warmer waters at night for feeding (Nakamura and Parin 1993; Zhang et al. 2016). This strong swimming ability is tied to the metabolic nature of the species. Zhang et al. (2017) showed that the Hairtail, with its high swimming capability, has a high expression of calcium cycling gene rates. Al Nahdi et al. (2016) suggest that hyperostosis might be adaptive, aiding in vertical water column movement for foraging in species like T. lepturus. However, they also contend that hyperostotic bones don´t cause a significant impact on an individual's center of mass and balance. Sun et al. (2020) showed that daily growth for juveniles of the species is closely linked to water temperature and nutrient availability. These seasonal variations – which last over long durations on a timescale – and daily variations, such as the vertical migration which is a short-term variation but has a broad range of temperature and pressure, should be factors considered in the propensity for developing the hyperostosis condition. The actual cause of hyperostosis development in marine teleosts remains unclear, requiring further studies on the influences of external factors and their roles in the metabolism of these species.

Numerous studies have identified hyperostosis in T.lepturus specimens, with the condition affecting various bone regions in fluctuating proportions. Our findings revealed an ontogenetic progression of this condition, suggesting it's associated with the aging process, in addition to the species-specific pattern. This is the first study to explore this development across different size classes for the Hairtail.

Conflict of interest. The authors have no competing interests to declare.

ACKNOWLEDGEMENTS

The authors would like to thank the entire radiographic team at “Diagnóstico Veterinário” for their support and for the radiographic images produced for this article. We thank Leonardo Giovanella for laboratory assistance.

DATA AVAILABILITY

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

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Description of Hyperostotic Bones Pattern in Hairtail Trichiurus lepturus

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Abstract

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1 INTRODUCTION

2 MATERIAL AND METHODS

2.1 Fish material

2.2 Radiology

2.3 Histology

3 RESULTS

4 DISCUSSION

CONCLUSION

Declarations

References

Additional Declarations

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