New records and range extension of two deep-sea skate genera, Amblyraja and Notoraja (Elasmobranchii: Rajiformes), in the southeastern Pacific Ocean

Abstract

Two species of deep-sea skates, Amblyraja frerichsi and Notoraja martinezi, are reported for the first time in Peruvian waters, representing the first record of their respective genera from the country. Earlier, A. frerichsi was known from both the southwestern Atlantic (off Brazil, Uruguay, and Argentina) and southeastern Pacific (off Chile), while N. martinezi was known from Costa Rica to Ecuador in the eastern-central and southeastern Pacific. This study contributes to the limited knowledge of deep-sea fish diversity along the South American west coast, and stresses the need of further taxonomic research in the region, particularly in light of the ecological importance of this group of fishes in marine ecosystems and its conservation state worldwide.

Introduction

Skates (Elasmobranchii: Rajiformes) are possibly the most diverse order of all cartilaginous fishes, with close to 300 species currently recognized (Fricke et al., 2023), and are found in all oceans, even including Antarctic waters (Duhamel et al., 2014; Weigmann, 2016). Three families and ten genera of skates have been reported in the southeastern Pacific Ocean: Bathyraja Ishiyama, 1958, Notoraja Ishiyama, 1958, Psammobatis Günther, 1870, and Sympterygia Müller & Henle, 1837 in Arhynchobatidae; Amblyraja Malm, 1877, Dipturus Rafinesque, 1810, Rajella Stehmann, 1970, Rostroraja Hulley, 1972, and Zearaja Whitley, 1939 in Rajidae; and Gurgesiella de Buen, 1959 in Gurgesiellidae (Concha et al., 2016; Last et al., 2016) – it is worth noting, however, that the validity of the genus Zearaja is still in debate (see Concha et al., 2019; Gabbanelli et al., 2022).

Only a half of the aforementioned genera is presently known from Peruvian waters (i.e. Bathyraja, Gurgesiella, Rajella, Rostroraja, and Sympterygia); nevertheless, it has been remarked that, given the relative paucity of studies focused on chondrichthyan taxonomy in the region, this number might be higher, particularly for deep-sea species inhabiting unfished or difficult to sample environments (Nakaya et al., 2009; Cornejo et al., 2015; Ebert, 2016). In the case of the deep-sea genera Amblyraja and Notoraja, while so far unknown from Peru, they have been recorded in the neighbouring countries of Chile, represented by Amblyraja frerichsi Krefft, 1968 (Bustamante et al., 2014), and Ecuador, represented by Notoraja martinezi Concha, Ebert & Long, 2016 (Calle-Morán and Béarez, 2020). Regarding Amblyraja, Ebert and Stehmann (2013) suggested that many species of its genus, including A. frerichsi, could correspond to variants of Amblyraja hyperborea (Collet, 1879), with the latter having taxonomic priority as the oldest name. Later molecular research has confirmed that Amblyraja badia (Garman, 1899), Amblyraja robertsi (Hulley, 1970), and probably Amblyraja jenseni (Bigelow & Schroeder, 1950) are indeed junior synonyms of A. hyperborea; however, A. frerichsi thus far remains a valid, distinct species (Last et al., 2016; Weigmann, 2016), and is treated here as such.

This paper documents the first known occurrence of A. frerichsi and N. martinezi in Peruvian waters, based on specimens caught during 2008 and 2016, extending the distribution range of both species and thus contributing to the limited knowledge of these fishes.

Materials and methods

In this study, results from samples collected by the Instituto del Mar del Perú (IMARPE) in two years, 2008 and 2016, are presented. First, in 2008, a study of the distribution, abundance, and biological characteristics of the fauna of the bentho-demersal subsystem (from 200 to 1500 m depth), and their relationship with the environmental conditions, was held on board the Spanish research vessel Miguel Oliver. Bottom trawling was used for the biological sampling, between 7°00′S and 10°00′S, off the coast of northern-central Peru. A fraction of the faunal specimens, including several skate species, were kept and preserved in the biological collection at IMARPE. Second, in October 2016, an exploratory fishing campaign with the participation of six vessels of the longline fleet targeting Patagonian toothfish Dissostichus eleginoides Smitt, 1898 was held, following IMARPE's guidelines. This fleet is made up of small-scale vessels, which have up to 32.6 m³ of hold capacity and are equipped with fishing equipment and systems that allow bottom longlines to reach depths of 900–2000 m depth. During this campaign, IMARPE's scientific technicians carried out biometric and biological sampling of the target species on board of each vessel, as well as recording the characteristics of the fishing activities in a logbook. Photographs and videos of species caught as bycatch (e.g. skates) were shot, and the specimens captured in the last two hauls per trip were preserved on ice and delivered to IMARPE's biological collection in Callao.

Species identification was carried out during recent efforts to review and catalogue IMARPE's growing fish collection, and was based on relevant literature, including original species' descriptions (Krefft, 1968; Concha et al., 2016; Ebert, 2016; Last et al., 2016). Morphometric measurements were carried out to the nearest millimetre following Last et al. (2008). Taxa are listed systematically following Van der Laan et al. (2014), while the taxonomic validity and current usage of species names follow Fricke et al. (2023).

Results

Class ELASMOBRANCHII
Order RAJIFORMES
Family ARHYNCHOBATIDAE Fowler, 1934
Genus Notoraja Ishiyama, 1958
Notoraja martinezi Concha, Ebert & Long, 2016

One specimen examined, a small male measuring 300 mm of total length (TL) (Figure 1), accession number IMARPE-013307, collected on 18 September 2008 by the R/V Miguel Oliver near Malabrigo, northern Peru (7°58.2′S, 80°35.8′W), at a depth of 1225–1227 m. Diagnostic characters include (1) disc heart-shaped and slightly wider (56.0% of TL) than long (51.7% of TL); (2) a long, slender tail, covered with numerous strong and posteriorly angled thorns, randomly aligned; (3) dorsal surface of disc mostly smooth except for dermal denticles scattered along its anterior margin and on either side of the midline; (4) a single, short, and strong preorbital thorn in front of each orbit; (5) anterior lobes of pelvic fins slim and longer than posterior lobes; and (6) dorsal and ventral surfaces dark brown in colour. Morphometrics and meristics are for the most part within the range of the type series, and further support the identification of the specimen as Notoraja martinezi (Table 1). The small, flexible claspers and the lack of alar thorns indicate that the studied individual is a juvenile.

Figure 1. N. martinezi Concha, Ebert & Long, 2016, preserved juvenile male IMARPE-013307 in (A) dorsal and (B) ventral views. Scale bar = 10 cm.

Table 1. Morphometric and meristic data of N. martinezi specimen IMARPE-013307, and type series

Data taken from Concha et al. (2016).

^a In male holotype specimen.

Family RAJIDAE de Blainville, 1816
Genus Amblyraja Malm, 1877
Amblyraja frerichsi Krefft, 1968

Two skates were observed in this study, a male and a female, caught on 22 October 2016, during the exploratory fishing campaign targeting Patagonian toothfish, near Ilo, southern Peru (17°45.0′S, 72°15.0′W), at a depth of 1605–1820 m. The male specimen, measuring 1040 mm TL (Figure 2), was preserved and deposited under the accession number IMARPE-019727 at IMARPE's biological collection; the female was discarded (footage recorded on board the fishing vessel showing both skates can be found in Supplementary Video S1). Both specimens were identified as Amblyraja frerichsi based on the following diagnostic characters: (1) thick, heavy body with a rhombic disc; (2) dorsal surface rough, abundantly covered with dermal denticles, thornlets, and thorns of various sizes; (3) thorn pattern consisting of two orbital, one spiracular, one nuchal, one mid-scapular, three scapular, and about 20 median thorns, the latter from behind scapular region to first dorsal fin; (4) tail shorter than disc length; (5) dorsal surface greyish brown with darker blotches and markings; (6) ventral surface almost uniformly dark brown, usually with lighter spots and blotches around snout, mouth, abdomen, pelvic fins, and cloaca. Morphometric measurements and meristic counts of the male specimen are mostly consistent with both those of the type series and with specimens from Chile (Table 2) – the large difference in clasper length is quite evidently due to Krefft's specimens being immature and bearing underdeveloped claspers. In this regard, our male specimen was determined to be an adult, possessing large, fully calcified claspers, as well as a complete patch of hook-like alar thorns on each pectoral fin. Being discarded, maturity could not be assessed for the female; however, its relatively large size (~1 m) suggests that it was also an adult, considering that all specimens over 965 mm TL in Bustamante et al.'s (2012) study were mature.

Figure 2. A. frerichsi Krefft, 1968, preserved adult male IMARPE-019727 in (A) dorsal and (B) ventral views. Scale bar = 30 cm.

Table 2. Morphometric and meristic data of A. frerichsi specimen IMARPE-019727, and comparative material, including type series

Data taken from Bustamante et al. (2012) and Krefft (1968).

^a For meristics, Krefft analysed 16 individuals.

Discussion

The specimens described herein represent the first documented records of each species in Peruvian waters. While distribution shifts in several marine species, including elasmobranchs, have been linked to anthropogenic factors such as climate change or artificial introduction (Perry et al., 2005; Bornatowski et al., 2018), this might not be the case for such deep-sea species, with habitat homogeneity being one of the key reasons for the relatively large depth and geographic ranges observed in these organisms, many of them cosmopolitan (McClain and Hardy, 2010; Costello and Chaudhary, 2017). Instead, what these new records probably represent is a dearth of adequate taxonomic studies in the region, added to the known difficulty in accurately identifying skate species (Cerutti-Pereyra et al., 2012; Ball et al., 2016). Indeed, both individuals had been earlier catalogued as ‘Bathyraja sp.’ in IMARPE's biological collection, and particularly with N. martinezi only being described in 2016, it was presumably very challenging for any non-specialist to correctly identify specimen IMARPE-013307 as a distinct taxon back in 2008.

The barbed wire-tailed skate, N. martinezi, the only species of Notoraja reported from the eastern Pacific Ocean, was heretofore known only from the four individuals described in Concha et al. (2016), consisting of one mature male and three immature female specimens, ranging from Costa Rica to Ecuador and collected at a depth between 1256 and 1472 m. The individual from Peru was found around 830 km (~8° of latitude) south of its geographically closest known specimen, the holotype (MEPN-18198) (top left; Figure 3), and at a slightly shallower depth (1225–1227 vs 1256–1308 m). Given the lack of additional records, it would appear that this is not a particularly common species, even if its distribution range is larger than originally assumed. Alternatively, it is possible that N. martinezi prefers even deeper waters, being abundant beyond current fishing grounds, as in the case of other softnose skates such as Bathyraja spinosissima Beebe and Tee-Van, 1941 (Ebert, 2016; Last et al., 2016). Furthermore, on a biological note, it is interesting to remark that in the Peruvian specimen (the only juvenile male known), the snout appears relatively shorter than that of the adult male holotype, and is more similar in shape to that of the female specimens depicted in the original description, suggesting secondary sexual dimorphism in the species, as Concha et al. (2016) hypothesize.

Figure 3. Map indicating the collection localities of N. martinezi specimen IMARPE-013307, and A. frerichsi specimen IMARPE-019727, both illustrated in blue. In black are the (as of prior to this study) southernmost record of N. martinezi, holotype specimen MEPN-18198, and northernmost record of A. frerichsi, reported in Ñacari et al. (2019).

Krefft (1968) described the thick body skate, A. frerichsi, on the basis of 34 specimens (the female holotype and 33 paratypes), collected off Argentina and Uruguay by the R/V Walther Herwig at a depth between 600 and 1000 m. Subsequently, it has been recorded near Rio de Janeiro (Gomes et al., 2019) and probably around the Falkland/Malvinas Islands (Bizikov et al., 2004; Pollom et al., 2021) in the Atlantic Ocean, and along much of the Chilean coast (Bustamante et al., 2012; Ñacari et al., 2019) in the Pacific. The records documented in this study represent a range extension of approximately 530 km (~5° of latitude) north of its earlier known distribution (bottom right; Figure 3). In contrast to N. martinezi, some additional records of A. frerichsi are known to the authors from Peruvian waters – albeit mostly uncatalogued specimens without precise coordinates, of which only photographic evidence remains, suggesting that this species might be a minor component of the bycatch of the Patagonian toothfish fishery that operates in the south of the country. This situation is in contrast to that of the Chilean D. eleginoides fishery, where A. frerichsi can constitute up to 97.5% of the total chondrichthyan bycatch (Reyes and Torres-Florez, 2009).

It should be mentioned that, even if new inclusions of fish species in national biodiversity lists might not be particularly relevant in purely biological terms because of the unnaturalness of countries' borders, they could be relevant conservation-wise. In Latin America, fisheries management, and particularly that of fisheries operating within national jurisdictions and exclusive economic zones, is mostly performed nationally via each country's fisheries authority, with management measures including, but not limited to, catch limits, fishing bans, minimum landing sizes, gear restrictions, and closed areas (Christy, 1997; Brown, 2017). Since understanding fisheries dynamics and characteristics, including the taxonomy and composition of their bycatch, has been identified as a crucial aspect for the conservation of chondrichthyans in Latin America (Becerril-García et al., 2022), the finding of N. martinezi and, specifically in this case, A. frerichsi, represents valuable information towards the goal of a continued increase in the knowledge and conservation of these and other deep-sea organisms that cohabit with high-value commercial species.

The diversity of deep-sea cartilaginous fish in the southeastern Pacific Ocean is a subject that remains understudied, despite the western coast of South America being one of the world's most productive fishing areas (Montecino and Lange, 2009). This study emphasizes the need for expanded research efforts in the region. Cartilaginous fishes, particularly skates, play numerous ecological roles in the marine ecosystem, and a decline in their populations could impact ocean communities at large (Flowers et al., 2021; Heithaus et al., 2022). This concern is heightened as over one-third of all chondrichthyans are currently threatened with extinction (Dulvy et al., 2021), and deep-sea ecosystems, in particular, face vulnerability to various human-induced impacts, including the expansion of bottom fisheries and plans for future mineral exploitation worldwide (Da Ros et al., 2019).