Introduction
Skates (Elasmobranchii: Rajiformes) are possibly the most diverse order of all cartilaginous fishes, with close to 300 species currently recognized (Fricke et al., Reference Fricke, Eschmeyer and Van der Laan2023), and are found in all oceans, even including Antarctic waters (Duhamel et al., Reference Duhamel, Hulley, Causse, Koubbi, Vacchi, Pruvost, Vigetta, Irisson, Mormède, Belchier, Dettai, Detrich, Gutt, Jones, Kock, Lopez Abellan, Van de Putte, De Broyer, Koubbi, Griffiths, Raymond, d'Udekem d'Acoz, Van de Putte, Danis, David, Grant, Gutt, Held, Hosie, Huettmann, Post and Ropert-Coudert2014; Weigmann, Reference Weigmann2016). 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., Reference Concha, Ebert and Long2016; Last et al., Reference Last, White, de Carvalho, Séret, Stehmann and Naylor2016) – it is worth noting, however, that the validity of the genus Zearaja is still in debate (see Concha et al., Reference Concha, Caira, Ebert and Pompert2019; Gabbanelli et al., Reference Gabbanelli, Naylor, Weigmann, Yang, Vazquez, Last, Díaz de Astarloa and Mabragaña2022).
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., Reference Nakaya, Yabe, Imamura, Romero and Yoshida2009; Cornejo et al., Reference Cornejo, Vélez-Zuazo, González-Pestana, Kouri and Mucientes2015; Ebert, Reference Ebert2016). 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, Reference Krefft1968 (Bustamante et al., Reference Bustamante, Vargas-Caro and Bennett2014), and Ecuador, represented by Notoraja martinezi Concha, Ebert & Long, Reference Concha, Ebert and Long2016 (Calle-Morán and Béarez, Reference Calle-Morán and Béarez2020). Regarding Amblyraja, Ebert and Stehmann (Reference Ebert and Stehmann2013) 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., Reference Last, White, de Carvalho, Séret, Stehmann and Naylor2016; Weigmann, Reference Weigmann2016), 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, Reference Krefft1968; Concha et al., Reference Concha, Ebert and Long2016; Ebert, Reference Ebert2016; Last et al., Reference Last, White, de Carvalho, Séret, Stehmann and Naylor2016). Morphometric measurements were carried out to the nearest millimetre following Last et al. (Reference Last, White, Pogonoski, Gledhill, Last, White, Pogonoski and Gledhill2008). Taxa are listed systematically following Van der Laan et al. (Reference Van der Laan, Eschmeyer and Fricke2014), while the taxonomic validity and current usage of species names follow Fricke et al. (Reference Fricke, Eschmeyer and Van der Laan2023).
Results
Class ELASMOBRANCHII
Order RAJIFORMES
Family ARHYNCHOBATIDAE Fowler, 1934
Genus Notoraja Ishiyama, 1958
Notoraja martinezi Concha, Ebert & Long, Reference Concha, Ebert and Long2016
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.
N. martinezi Concha, Ebert & Long, Reference Concha, Ebert and Long2016, preserved juvenile male IMARPE-013307 in (A) dorsal and (B) ventral views. Scale bar = 10 cm.
Morphometric and meristic data of N. martinezi specimen IMARPE-013307, and type series
Data taken from Concha et al. (Reference Concha, Ebert and Long2016).
a In male holotype specimen.
Family RAJIDAE de Blainville, 1816
Genus Amblyraja Malm, 1877
Amblyraja frerichsi Krefft, Reference Krefft1968
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 (Reference Bustamante, Lamilla, Concha, Ebert and Bennett2012) study were mature.
A. frerichsi Krefft, Reference Krefft1968, preserved adult male IMARPE-019727 in (A) dorsal and (B) ventral views. Scale bar = 30 cm.
Morphometric and meristic data of A. frerichsi specimen IMARPE-019727, and comparative material, including type series
Data taken from Bustamante et al. (Reference Bustamante, Lamilla, Concha, Ebert and Bennett2012) and Krefft (Reference Krefft1968).
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., Reference Perry, Low, Ellis and Reynolds2005; Bornatowski et al., Reference Bornatowski, Loose, Sampaio, Gadig, Carvalho-Filho and Domingues2018), 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, Reference McClain and Hardy2010; Costello and Chaudhary, Reference Costello and Chaudhary2017). 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., Reference Cerutti-Pereyra, Meekan, Wei, O'Shea, Bradshaw and Austin2012; Ball et al., Reference Ball, Serra-Pereira, Ellis, Genner, Iglésias, Johnson, Jones, Leslie, Lewis, Mariani, Menezes, Neat, Noble, Sims and Griffiths2016). 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. (Reference Concha, Ebert and Long2016), 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, Reference Ebert2016; Last et al., Reference Last, White, de Carvalho, Séret, Stehmann and Naylor2016). 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. (Reference Concha, Ebert and Long2016) hypothesize.
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. (Reference Ñacari, Sepúlveda, Escribano and Oliva2019).
Krefft (Reference Krefft1968) 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., Reference Gomes, Santos, Gadig, Signori and Vicente2019) and probably around the Falkland/Malvinas Islands (Bizikov et al., Reference Bizikov, Arkhipkin, Laptikhovsky and Pompert2004; Pollom et al., Reference Pollom, Dulvy, Acuña, Bustamante, Chiaramonte, Cuevas, Herman, Paesch, Pompert and Velez-Zuazo2021) in the Atlantic Ocean, and along much of the Chilean coast (Bustamante et al., Reference Bustamante, Lamilla, Concha, Ebert and Bennett2012; 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, Reference Reyes and Torres-Florez2009).
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, Reference Christy1997; Brown, Reference Brown2017). 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., Reference Becerril-García, Arauz, Arellano-Martínez, Bonfil, Ayala-Bocos, Castillo-Géniz, Carrera-Fernández, Charvet, Chiaramonte, Cisneros-Montemayor, Concha, Espinoza, Ehemann, Estupiñán-Montaño, Fuentes, Galván-Magaña, Graham, Hacohen-Domené, Hazin, Hernández, Hoyos-Padilla, Ketchum, Kingma, Méndez, Oddone, Pérez-Jiménez, Petatán-Ramírez, Polo-Silva, Rangel, Salinas-De-León, Santana-Morales, Zanella, Vélez-Zuazo and Godard-Codding2022), 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, Reference Montecino and Lange2009). 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., Reference Flowers, Heithaus and Papastamatiou2021; Heithaus et al., Reference Heithaus, Dunn, Farabaugh, Lester, Madin, Meekan, Papastamatiou, Roff, Vaudo, Wirsing, Carrier, Simpfendorfer, Heithaus and Yopak2022). This concern is heightened as over one-third of all chondrichthyans are currently threatened with extinction (Dulvy et al., Reference Dulvy, Pacoureau, Rigby, Pollom, Jabado, Ebert, Finucci, Pollock, Cheok, Derrick, Herman, Sherman, VanderWright, Lawson, Walls, Carlson, Charvet, Bineesh, Fernando, Ralph, Matsushiba, Hilton-Taylor, Fordham and Simpfendorfer2021), 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., Reference Da Ros, Dell'Anno, Morato, Sweetman, Carreiro-Silva, Smith, Papadopoulou, Corinaldesi, Bianchelli, Gambi, Cimino, Snelgrove, Van Dover and Danovaro2019).
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0025315424000122
Data
The authors confirm that the data supporting the findings of this study are available within the article.
Acknowledgements
The authors thank the crew of the R/V Miguel Oliver 2008 and everyone who participated in the collection of biological material and field work, especially biologist Miguel Romero. We also thank biologist Renato Guevara, Scientific Executive Director of IMARPE, and biologist Elisa Goya, head of IMARPE's Biodiversity Area for the interest, support, and for allowing the use of the research facilities. Lastly, we thank fisheries biologist Jesus Buleje Alfaro for recording Supplementary Video S1 and providing the specimen of A. frerichsi to IMARPE's collection in 2016.
Author's contribution
F. Z., I. C., S. C.-L.: conceptualization, methodology, formal analysis, investigation, resources, data curation, writing (original draft), figures, and tables. A. M.-M.: formal analysis, investigation, resources, writing (review and editing). M. S.: methodology, formal analysis, resources, writing (review and editing); was also in charge of IMARPE's Patagonian toothfish exploratory fishing guidelines in 2016. All authors read and approved the final manuscript.
Financial support
This study was supported by the Instituto del Mar del Perú (IMARPE).
Competing interests
None.
Ethical standards
The authors declare that they have not violated or omitted ethical or legal norms when carrying out the research for this study. The Instituto del Mar del Perú (IMARPE), being an affiliated scientific research institute, does not need to request permission from the governing body, the Ministry of Production (PRODUCE), for the collection of samples. Sampling was not carried out within any National Protected Area. No experiments or procedures were performed on live animals.
