First records of  Chionodraco hamatus  nests in coastal areas of Terra Nova Bay (Ross Sea): a potential nesting area for the species?

doi:10.21203/rs.3.rs-3101138/v1

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First records of Chionodraco hamatus nests in coastal areas of Terra Nova Bay (Ross Sea): a potential nesting area for the species?

https://doi.org/10.21203/rs.3.rs-3101138/v1

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Nests of the icefish Chionodraco hamatus were documented for the first time at about 500 m depth at Terra Nova Bay (Victoria Land, western Ross Sea), in an area included in the Antarctic Specially Protected Area (ASPA) No. 173 and in the portion with more stringent protection of the largest established marine protected area of the world, the Ross Sea Region Marine Protected Area (RSRMPA). Nest building and eggs guarding are common parental care behaviours in the Antarctic icefishes (Channichthyidae). Prior to present work, nest building behaviour for C. hamatus was observed only in the frame of aquarium experiments.

Here we report on the observation of five nests of C. hamatus by remote underwater video systems in November 2021, during an Italian Antarctic expedition. The nests, consisting of gravel and small stones, were circular and bowl-shaped with a consistent diameter of about 30–40 cm. Nest building behaviour, with the icefish individual alternating radial turns in clockwise and counter-clockwise movements was also recorded in situ for the first time. By considering the occurrence of the icefish nests, as well as biotic and abiotic features of the locality, the existence of a C. hamatus nesting area is hypothesised. If confirmed, the occurrence of an icefish nesting area in Silverfish Bay would further strengthen the ecological value of the ASPA 173. Furthermore, documenting nesting icefish in nearshore coastal areas of the RSRMPA reinforces the relevance of the MPA itself and provides an important focus for future research and monitoring in the area.

Icefish

Nesting area

Ross Sea Region MPA

Remote visual techniques

In the Southern Ocean, the largest marine protected area of the world - the Ross Sea region MPA (RSRMPA) - was established in 2016 under the Commission for Conservation of Antarctic Marine Living Resources (CCAMLR). This vast MPA encompasses a wide variety of marine environments, from shelf to slope waters. According to the CCAMLR Conservation Measure 91 − 05, the RSRMPA is designed to address a number of specific objectives, including the conservation of natural ecological structure, dynamic and function (objective i), the conservation of biodiversity through protection of representative portions of benthic and pelagic marine environments in areas where fewer data exist (objective iv), and the protection of coastal locations of particular ecological importance (objective viii). In this context, scientific efforts are required to improve current knowledge of understudied areas, in support of the aims of the RSRMPA Research and Monitoring Plan. These areas include the nearshore coastal region of Victoria Land, known to support diverse seafloor habitats and communities of considerable ecological importance to the Ross Shelf ecosystem (Thrush et al. 2006). Prior to the establishment of the RSRMPA, the high ecological value of some coastal areas of the Victoria Land, led to the establishment of ASPAs (Antarctic Specially Protected Areas) under the Protocol on Environmental Protection to the Antarctic Treaty.

In 2013, the ASPA No. 173 Cape Washington & Silverfish Bay was designed in northern Terra Nova Bay, a coastal area where the sea ice persists from March to January, including one of the largest emperor penguin (Aptenodytes forsteri) colonies and the first documented, and until now the only known, nursery and hatching area of the Antarctic silverfish (Pleuragramma antarcticum), a keystone species of the Antarctic marine ecosystem (Vacchi et al. 2012). Despite the great ecological value of this ASPA, very little is known about the communities of marine organisms associated with the seafloor at depths between 200 and 500 metres.

Given the presence of sea ice (particularly fast ice) for most of the year, understanding of the coastal biogeography and ecosystem processes is limited to a restricted number of areas at depths accessible by dive-based operations (Cummings et al. 2018). Such constraints are being overcome by the use of remote visual techniques, which are emerging as low-impact tools for collecting visual information on fish and benthic communities (Castellan et al. 2021). In recent years, visual methodologies have been applied worldwide to improve current knowledge on the spatial patterns of biodiversity, substantially contributing to ecosystem monitoring and management of MPAs (Cappo et al.2003; Jessop et al.2022). Indeed, remote visual techniques can greatly help investigations of data-poor areas, allowing the characterisation of marine communities, and documentation of unique features, such as the case of the recently discovered vast icefish (Neopagetopsis ionah) breeding colony in the Weddell Sea (Purser et al. 2022). In the Ross Sea, recent pilot studies on the presence and abundance of Antarctic toothfish (Dissostichus mawsoni) in sea ice-covered continental shelf areas (O’Driscoll et al. 2018; Di Blasi et al. 2021) have highlighted the potential use of remote visual techniques to explore the environment and marine communities in such areas.

The fish fauna of the Ross Sea is overwhelmingly dominated, in terms of diversity and biomass, by the suborder Notothenioidei (La Mesa et al. 2004) in four families: Artedidraconidae, Bathydraconidae, Channichthyidae, and Nototheniidae (Eastman and Eakin 2021). Those families are well represented also in the coastal fish community of Terra Nova Bay, where the channichthyid Chionodraco hamatus is one of the most abundant species (Vacchi et al. 2000; La Mesa et al. 2022). This benthic fish species is widespread in the High Antarctic zone (areas covered by pack ice for most of the year), inhabiting a wide range of depths from the surface to about 600 m (Gon and Heemstra 1990; Vacchi et al. 1996). The icefish family (Channichthyidae), exhibiting unique biological and ecological characteristics, such as the absence of haemoglobin, has been extensively studied (reviewed in Kock 2005). However, information on key ecological and biological issues, including reproductive strategies and areas, is sparse (Detrich et al 2005; Jones and Near 2012; Ferrando et al. 2014; Riginella et al. 2021). Species of this family generally spawn in spring or summer, and are characterised by low fecundity, large egg size at spawning and large larvae at hatching (Koch and Kellermann 1991; La Mesa et al. 2020); characteristics which are considered representative of the initial stage towards the development of parental care (Riginella et al. 2021). Parental care is one of the most common strategies to improve offspring survival and fitness, carried out through various activities: building, cleaning the nest and eggs guarding until hatching (Gross 2005; Balshine and Sloman 2011).

About 20 Antarctic notothenioid species are known to exhibit forms of parental care and nesting; among them, the family Channichthyidae include the largest number of genera exhibiting nesting behaviour, namely Neopagetopsis, Pagetopsis, Chaeonodraco, Chionodraco, Chaenocephalus and Chionobathyscus (La Mesa et al. 2020; Purser et al. 2022). Most of the data on parental care and nesting behaviour were collected in the field during surveys carried out by research vessels. Due to logistical constraints related to the seasonal accessibility of High-Antarctic coastal areas, nest building and egg guarding in C. hamatus have only been documented ex situ in the frame of aquarium experiments (Ferrando et al. 2014). Here we report on the first record of C. hamatus icefish nests in the Ross Sea region, at about 500 m depths at Silverfish Bay, an area included in the ASPA No.173 and in the RSRMPA.

Terra Nova Bay is a coastal area of Victoria Land (western Ross Sea; RSRMPA, General Protection Zone) bounded to the north by Cape Washington and to the south by the Drygalski Ice Tongue (Fig. 1a). The Drygalski Ice Tongue, the Nansen Ice Sheet and the Campbell Glacier Tongue descend from the continent toward the bay. The coastline is indented with embayments, including Gerlache Inlet and Silverfish Bay in the northern part, with an average depth of about 500 metres and irregular bottom topography, characterized by steep bottoms consisting of granitic rock ridges and gullies filled with gravel, clay, and silt (Vacchi et al. 2012; Di Blasi et al. 2021). The study area, in the ASPA No. 173 Cape Washington & Silverfish Bay (Fig. 1a) is a coastal area of 286 km² of which 279.5 km² are marine (98%) and 6.5 km² are terrestrial (2%), where fast-ice persists from March to January.

C. hamatus nests were discovered by chance during a visual survey in November 2021 (Fig. 1b), as part of a project investigating the distribution and monitoring of Antarctic toothfish using Baited Remote Underwater Video systems (BRUVs).

The mini-BRUV system was designed ad hoc and deployed from holes in the sea ice. Details on the baited camera system are reported in Di Blasi et al. 2021. The camera configuration was vertical with the view towards the seafloor, resulting in a field of view of about 2 m in diameter. Five stations were visited, representative of different geomorphological features in a depth range from less than 200 m to more than 500 m (Fig. 1b; Table 1).

Table 1

Stations investigated by means of BRUV at Silverfish Bay in November 2021
Station	Date	Latitude	Longitude	Depth	Geomorphology	Substrate
A	02/11/2021	74°40.585 S	164°47.959 E	475 m	trench	soft
B	11/11/2021	74°39.585 S	164°40.501 E	543 m	trench	soft
C	15/11/2021	74°38.031 S	164°41.351 E	454 m	trench	soft
D	08/11/2021	74°39.613 S	164°46.132 E	356 m	ridge	soft
E	09/11/2021	74°38.026 S	164°46.161 E	179 m	ridge	hard

During the XXXVII Italian Antarctic Expedition, nests of the icefish C. hamatus were observed for the first time in Silverfish Bay (Terra Nova Bay, Ross Sea). The nests were observed at three out of the five sampled stations (St. A, B and D), at depths of 356 m, 475 m, and 543 m in soft bottom areas (Fig. 1b; Table 1).

The nests, circular and bowl-shaped, consisted of gravel and small stones. Based on the adult individuals’ average length for the species (Gon and Heemstra 1990), the nest diameter was estimated to be about 30–40 cm. The bowl-shaped depression form of nests is the most common in fish and has also been observed in other icefish species (Detrich et al. 2005; Purser et al. 2022). Such a shape is hypothesized to prevent the eggs from being transported laterally outside the nests by the benthic current, while the nest material, gravel and small stones, maintains adequate aeration (Detrich et al 2005; Purser et al. 2022).

In station A (Fig. 2a), three nests were observed: one with an adult icefish individual positioned above the centre of the nest, and the other two nests empty. However, four fish were observed in the proximity of empty nests.

Similarly, one empty nest was observed at station B (Fig. 2b), with one individual in the same field of view. In station D, one icefish individual was observed performing alternate clockwise and counter-clockwise radial movements. The circle drawn on the substrate had a diameter approximately corresponding to the fish body length. During the turns, the icefish was sweeping the sea-floor by vibrating its pelvic and anal fins with an intense and continuous wave-like motion. This behaviour had been observed previously for the species in captive-bred fish, where nesting activities were recorded during the pre-spawning phase, the most intense substrate sweeping being performed by males on the day before spawning (Ferrando et al. 2014).

In fish species characterized by external fertilization, it is usual that males show parental care (Gross and Sargent 1985). Sexual dimorphism in size and morphology is widespread among teleosts, is documented in several icefish species, including C. hamatus (Koch 2005; Ferrando et al. 2014), and is often related to parental care and nest construction behaviour of males (Mank et al. 2005; Balshine and Sloman 2011; La Mesa et al. 2020). In the mature males of the two Chionodraco species, C. hamatus and C. rastrospinosus, temporary white fleshy, club-like modifications of their anal fins, covered by a thick epithelium, were found during the breeding season (Ferrando et al. 2014). These anal fin modifications can facilitate nest building activities, and their continuous movement allows the icefish to maintain the nest free of sand or debris (Ferrando et al. 2014). Such morphological characteristics were visible in some of the individuals observed in the field, that were therefore identified as males.

C. hamatus is typically a summer spawner, with peak spawning occurring between January and February (Vacchi et al.1996; La Mesa et al. 2011). This is consistent with our observation of males engaged in pre-spawning activities, selection of an appropriate location and nest building. The latter is a key activity for successful reproduction, since a properly-placed and well-constructed nest supports the development of the offspring (Balshine and Sloman 2011).

Parental care is particularly important for species, such as the Channichthyidae, with demersal eggs that can easily be predated by benthic organisms, such as starfish and other fish species (Kock et al. 2006). Here, we observed sparse benthic organisms in proximity to the nests, with the dominance of echinoderms, especially starfish, and polychaete annelids, such as serpulids, very common benthic fauna associated to soft bottoms of the shelf. Additional benthopelagic fish species were observed in association with nests, including adult Antarctic toothfish, juvenile Antarctic silverfish, and other species of the Nototheniidae family. Silverfish Bay is known to host a nursery site of Antarctic silverfish, and recent studies on Antarctic toothfish have confirmed the presence of this large predator in the area (O’Driscoll et al. 2018; Di Blasi et al. 2021). Early silverfish larvae dominate the diet of C. hamatus larvae and postlarvae in the western Ross Sea (La Mesa et al. 2011), therefore the icefish nest building and egg deposition in this area may not only be related to the sea bottom characteristics, but also to the biotic features of the area.

The presence of icefish nests, as well as biotic and abiotic features of the locality, suggest the existence of a C. hamatus nesting area. If confirmed, the occurrence of an icefish nesting area in Silverfish Bay would further strengthen the ecological value of the ASPA No. 173. Further research, using low-impact sampling methods such as remotely operated vehicles (ROVs) surveys or towed camera systems surveys, is needed to investigate the presence, spatial extent, and environmental characteristics of this potential nesting area. Documenting nesting icefish in nearshore coastal areas of the RSRMPA reinforces the relevance of the MPA itself, and provides an important focus for guiding future research and monitoring in the area.

Acknowledgements

We thank the Italian National Programme for Antarctic Research (PNRA) for having supported the project MIUR-PNRA2018_00016 - DISCOVERY “Monitoring Dissostichus mawsoni in sea-ice covered areas of the Ross Sea Region MPA by low-impact technologies”. We are very grateful for the excellent and crucial technical support provided by Giacomo Bonanno (ENEA Casaccia, Rome). Present work contributes to the SCAR-AntICON Programme (Integrated Science to Inform Antarctic and Southern Ocean Conservation) to answer key scientific questions (identified by the SCAR Horizon Scan) related to the conservation and management of Antarctica and the Southern Ocean.

Author contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Laura Ghigliotti, Simonepietro Canese, Davide Di Blasi and Erica Carlig. The first draft of the manuscript was written by Erica Carlig and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript

Funding This study was funded by the Italian National Programme for Antarctic Research (project MIUR-PNRA2018_00016 - DISCOVERY).

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

Conflict of interest The authors declare no conflict of interest.

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Editorial decision: Acceptable after minor revision
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First records of Chionodraco hamatus nests in coastal areas of Terra Nova Bay (Ross Sea): a potential nesting area for the species?

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