Abstract
The Shortnose Guitarfish, Zapteryx brevirostris , is endemic to the Southwest Atlantic and its geographic range is commonly reported from Southeastern Brazil to Northern Argentina. However, range limits are imprecise or inconsistent in some cases. These inconsistencies were addressed in this study based on 1,363 specimens collected since 1865. These records were obtained from scientific collections, a systematic review of literature, and an on-board observation database. According to the data collected in this study, the known northernmost distributional limit of the species lies at the mouth of the Doce River, Northern Espírito Santo State, in Southeastern Brazil (19°S). As for the other extreme of its range, the known southernmost distribution limit refers to the Falkland Islands (Malvinas) (53°S). This represents more than 2,000 km of coastline geographic range extension — in comparison to the previous known southernmost range limit for this species. The geographical range of Z. brevirostris seems to follow biogeographic patterns operating at an ecosystem level in which biotic (especially in the north) and abiotic factors (especially in the south) play a role in imposing limits to its distribution range.
Keywords:
Batoid; Chondrichthyes; Distribution range; Range boundaries; Southwest Atlantic Ocean
INTRODUCTION
Distributional limits of species are influenced by many factors in a complex interaction system (Brown and Lomolino, 1998 , Lomolino et al., 2010 ). These include ecological and environmental factors, such as biotic interactions and abiotic conditions (Dobzhansky, 1950 , MacArthur, 1972 ), as well as evolutionary responses to biotic and abiotic gradients (Hardie and Hutchings, 2010 , Willi and Van Buskirk, 2019 , Alexander et al., 2022 ). Besides being an issue of biological interest due to connecting species range to ecology and evolution, understanding species boundaries may also be crucial information considering global environmental changes (Thomas, 2010 ). As global temperatures fluctuate and habitats undergo transformations, certain species may migrate or adapt, whereas others may face higher extinction risks (Gervais et al., 2021 ). Furthermore, understanding the geographic range of a species and shifts on its boundaries is fundamental for conservation planning (Franklin, 2010 ). For instance, a well-defined geographic range may help establish priority conservation areas, appropriate monitoring of range reduction, and overlapping threats (Chan et al., 2021 , Becerril-García et al., 2022 ). Therefore, establishing well-defined geographic range and distributional limits of species at risk of extinction can be considered a pressing issue.
Currently, one of the most threatened groups of species in the world is the Elasmobranchii, which includes sharks and rays (Díaz et al., 2019 ). Bycatch, overexploitation, and finning have led to population declines of dozens of species (Dulvy et al., 2014 , Dent and Clarke, 2015 , Charvet et al., 2021 , Dulvy et al., 2021 ). Many elasmobranchs are characterized by slow growth, late maturity, and low fecundity, which make this group much more susceptible to threats (Dulvy et al., 2014 ). Among them, shark-like batoids (Rhinopristiformes) are one of the most threatened groups (Faria et al., 2013 , Moore, 2017 , Jabado, 2018 , Dulvy et al., 2021 ). The genus Zapteryx Jordan and Gilbert, 1880 comprises three batoid species of the order Rhinopristiformes (Last et al., 2016 , Weigmann, 2016 ). One of them, the Shortnose Guitarfish Zapteryx brevirostris (Müller and Henle, 1841) is endemic to the Southwest Atlantic from Southeastern Brazil to Northern Argentina (Weigmann, 2016 , Gomes et al., 2019 ).
This trygonorrhinid batoid has a short cuneiform-shaped snout, which is the main morphological character to differ it from other guitarfishes from the Southwest Atlantic (Last et al., 2016 ). The only somewhat similar guitarfishes in this region include two rhinobatid species, Pseudobatos horkelii (Müller and Henle, 1841) and P. percellens (Walbaum, 1792), which differ from Z. brevirostris because they have an elongated snout (Bigelow and Schroeder, 1953 ). The Shortnose Guitarfish is commonly caught as bycatch throughout its geographic range (Costa and Chaves, 2006 , Chiaramonte et al., 2011 , Colonello et al., 2011 , Wosnick et al., 2019 ). This led to a population reduction of 85% in Brazil and 25% in Uruguay in the last three generations period (Pollom et al., 2020 ). Consequently, this species is currently listed as Endangered (EN) by the International Union for Conservation of Nature (IUCN) Red List of Threatened Species (Pollom et al., 2020 ). Its current conservation status suggests a trend of increased extinction risk given that in its previous IUCN Red List assessment this species was assigned to a lower threat category (Vulnerable - VU; Vooren et al., 2006 ).
Within the geographic range of Z. brevirostris , there currently exists some confusion about its distributional limits. Historically, the northernmost limit has been mentioned as the oceanic Fernando de Noronha Archipelago (Northeastern Brazil) (Batista, 1987a , 1987b , Castello, 1971 , Santos et al., 2006 , but not in Soto, 2001 ), Bahia State (Northeastern Brazil) (Bigelow and Schroeder, 1953 , Menni and Stehmann, 2000 ), Espírito Santo State (Southeastern Brazil) (Pinheiro et al., 2015 ; Pollom et al., 2020 ), and Rio de Janeiro State (Southeastern Brazil) (Miranda-Ribeiro, 1904 , 1907 ). On the other hand, the southernmost limit has more consistently been mentioned as Mar del Plata (Argentina) in the literature (Menni and Stehmann, 2000 , Wosnick and Freire, 2013 , Gomes et al., 2019 , Wosnick et al., 2019 ), although one online database (i.e., FishBase) reports one specimen collected as south as the Falkland Islands (Malvinas) (Froese and Pauly, 2022 ). [The Falkland Islands (Malvinas) are listed as a Non-Self-Governing Territory by the United Nations, which also recognizes the dispute concerning the sovereignty of these islands (UN, 2024 ).] This study reviewed the occurrence records of Z. brevirostris along its geographic range, focusing on its distributional limits.
METHODS
Occurrence records of Z. brevirostris were first compiled from two sources. Specimens deposited in scientific collections were accessed by (1) online database search made on SpeciesLink (SpeciesLink, 2022 ) and Global Biodiversity Information Facility-GBIF (GBIF, 2022 ) and (2) inquiries to curators and collection managers from museums and scientific collections ( Table 1 ). The taxonomic identification associated with specimen records obtained from online databases was considered reliable since Z. brevirostris is the only species of the family in the Atlantic Ocean (Weigmann, 2016 ). In one case, additional information and photographs from a female specimen from the Falkland Islands (Malvinas) (ISH 591-1978, a specimen from the Zoologisches Museum, Universität Hamburg, ZMH collection) was obtained to verify the species identity and associated locality information.
Museums and scientific collections used as source of occurrence records of the Shortnose Guitarfish, Zapteryx brevirostris . The left column indicates how the locality information associated with specimens were accessed. The right column shows the collections that served as source of information; codes follow Fricke and Eschmeyer ( 2023 ), Sabaj (2022), and Faria et al. ( 2021 ).
Another source of information of occurrence records of Z. brevirostris was a systematic review of literature. For this, the PICO Strategy (acronym for patient/population, intervention, comparison, and outcome) was applied to the bibliographic search, according to a previously described methodology (Richardson et al., 1995 ). The terms ‘population’ and ‘intervention’ were used to choose keywords (O’Dea et al., 2021 ). In the search, under ‘population’ the term searched was ‘ Zapteryx brevirostris ,’ and, under ‘intervention,’ the term ‘Atlantic’ was applied in three languages (English, Portuguese, and Spanish). The Boolean operator AND was applied to combine the terms ‘population’ and ‘intervention.’ The term ‘Atlantic’ (three languages) was separated by the Boolean operator OR.
The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) is a set of guidelines and a structured framework for planning and conducting systematic reviews and meta-analyses in research (O’Dea et al., 2021 ). The PRISMA Protocol approach was used as the criteria for research article selection. Searches using the online databases Scopus, ScienceDirect, and Web of Science were carried out on May 15, 2023. Additional searches in Google Scholar using the term ’ Zapteryx brevirostris’ as keyword were carried out for further information about geographic range and distributional limits of Z. brevirostris . Only research articles and one technical note that provided primary occurrence data of Z. brevirostris were included in the analysis. Conversely, articles providing only secondary or incomplete occurrence data of Z. brevirostris and those providing occurrence data of other Zapteryx species were excluded.
One last source of information was the ‘On-Board Observer Program’ of the Fisheries Secretariat of the Province of Chubut, Argentina. This program monitors bycatch in the Pleoticus muelleri (Bate, 1888) shrimp fishery. This database has been kept unpublished but was accessed by the second author of this study (N. Bovcon).
For map preparation, the geographic range of Z. brevirostris , geographic coordinates, and shapefiles were converted to WGS84. Then, occurrence records with inaccuracies or missing coordinates were removed from the dataset. Records without geographic coordinates but with detailed information about the sampling locality had the coordinates estimated and were included in the dataset used for map construction. Once the dataset was considered suitable, the geographic coordinates were plotted on Qgis, version 3.10.8 (QGIS, 2020 ).
RESULTS
Data collection resulted in 1,363 specimens of Zapteryx brevirostris: one from on-board observation, 257 from scientific collections, and 1,105 from the literature review (30 research articles and one technical note) from 1865 to 2022 ( Table S1 ; Supplementary Material). These specimens were collected from 107 localities - each considered an occurrence point - from Brazil, Uruguay, and Argentina ( Figure 1 ). The 107 occurrence points had the following sources: collection managers (n = 16), online databases (n = 80), published research articles (n = 9), on-board observation (n = 1), and a technical note (n = 1).
The search for Z. brevirostris on the three databases (Scopus, ScienceDirect, and Web of Science) resulted in 42 research articles that mentioned the occurrence of this species, 25 of which were excluded from this study due to duplicates and lack of precise occurrence data, which resulted in 17 research articles being considered suitable. Moreover, 13 research articles were incorporated after a complementary search (i.e., Google Scholar). Therefore, 30 research articles were effectively included in this study (references in Table 2 and as follows: Jaureguizar et al., 2003 , 2004 , Colonello et al., 2014 , Loto et al., 2018 , Alvarenga et al., 2021 , Gatts et al., 2021 , Karlovic et al., 2021 , Lucena et al., 2021 , Martins et al., 2021 , Takatsuka et al., 2022 ). These 30 research articles reported data from each country as follows: Brazil only (n = 23); Brazil, Uruguay, and Argentina (n = 1); Argentina and Uruguay (n = 3); and Argentina only (n = 3) ( Table S1 ). All studies included provided information on geographic range or distributional limits or information, such as sampling location and/or number of individuals.
Dot map of the geographic range of the Shortnose Guitarfish, Zapteryx brevirostris . Each black dot represents a locality in which the species has been documented by either a voucher deposited in museums and scientific collections or a specimen mentioned in a scientific article. The red star represents the species northernmost occurrence: Linhares, in 2016 (voucher specimen MBML–PEIXES 120490). Red triangles represent the species southernmost occurrence: (1) upper triangle: Chubut, in 2010 (on-board observation; N. D. Bovcon, unpubl. data); (2) the triangle in between the other two: Santa Cruz Province, in 1997 (technical note; Wöhler et al., 1999 ) and (3) the lower triangle: south of the Falkland Islands (Malvinas), in 1978 (voucher specimen ISH 591-1978). Oceanographic currents follow Piola and Matano ( 2019 ). ES: Espírito Santo State.
List of publications that included specific remarks on the geographic range or distributional limits associated with the Shortnose Guitarfish, Zapteryx brevirostris .
The northernmost records for Z . brevirostris refer to three specimens captured at the mouth of the Doce River, Regência, in the Municipality of Linhares, Northern Espírito Santo State, Southeastern Brazil (19°44’57” S 39°41’51” W; MBML – PEIXES 12049). Other northernmost records of Z. brevirostris include an adult female from Aracruz, Espírito Santo State (19°49’49” S 40°03’09” W; CIDRO-B-38; Figure ¿fig:2A? ) and a juvenile male from Piúma, Espírito Santo State (20°50’ 58”S 40°43’56” W; CIDRO-B-39; Figure ¿fig:2B? ).
Three voucher specimens of the Shortnose Guitarfish, Zapteryx brevirostris , collected at the species distributional limits. Figure 2 A: dorsal view of an adult female from Aracruz, Espírito Santo State, Southeastern Brazil (CIDRO-B-38; photo by Lilian Xavier). Figure 2 B: dorsal view of a juvenile male from Piúma, Espírito Santo State, Southeastern Brazil (CIDRO-B-39; photo by Lilian Xavier). Figure 2 - C1 and Figure 2 - C2: dorsal and ventral views, respectively, from an adult female from the Falkland Islands (Malvinas) (ISH 591-1978; photos by Irina Eidus). Scale bar: 10 cm.
The southernmost records for Z. brevirostris were as follows: (1) one specimen captured in the coastal area of the Province of Chubut, Argentina (43°30’S 65°12’W; 34 m depth, December 26, 2010) as part of the ‘On-Board Observer Program’ of the Fisheries Secretariat of the Province of Chubut, which monitors bycatch in the Pleoticus muelleri (Bate, 1888) shrimp fishery (Bovcon, unpubl. data); (2) one specimen captured in the Province of Santa Cruz, Argentina (48°28.3’S 65°24.5’W; from 50–100 m depth isobaths) in 1997 during research campaigns for southern demersal fisheries carried out in the summer on the continental shelf of the Argentine Sea by the National Institute for Fisheries Research and Development - INIDEP (Wöhler et al., 1999 ); and (3) one specimen captured south of the Falkland Islands (Malvinas) (53°52’S 59°55’W; 205 m depth) as part of the Argentine Expedition 1978 (ISH 591-1978, this specimen is currently deposited at the Zoologisches Museum, Universität Hamburg; Figure 2 - C1 and C2 - Table S1 ).
DISCUSSION
The geographic distribution of species is often associated to patterns delimited as biogeographic provinces (Briggs, 1974 ). Delimiting a biogeographic province follows distinct criteria in different approaches; as a result, its limits and names fail to necessarily coincide (e.g. Spalding et al., 2007 , Toonen et al., 2016 ). Furthermore, the distributional limits of species fail to be always restricted to a single biogeographic province (Spalding et al., 2007 , Briggs and Bowen, 2012 ). This seems to be the case regarding the distribution of Z apteryx brevirostris , which can be associated with various provinces: (a) Indian (Indias Occidentales), Temperate Western South Atlantic (Argentina), and Magellanic (Magallánica) ( sensu Lopez, 1963 , Menni and Stehmann, 2000 , Menni et al., 2010 , Cousseu et al., 2020 ); (b) also Brazilian, Argentinian, Southern Argentina, and Falkland Islands ( sensu Floeter et al., 2008 , Briggs and Bowen, 2012 , Toonen et al., 2016 ); (c) and Tropical Southwestern Atlantic, Warm Temperate Southwestern Atlantic, and Magellanic ( sensu Spalding et al., 2007 ). Regardless of which approach is followed, in all cases, this species crosses different biogeographical limits and its distribution range comprises at least three biogeographical provinces.
Zapteryx brevirostris uses multiple marine habitats (Barbini et al., 2011 ), including estuaries (Wosnick and Freire, 2013 ), which may favor its dispersion from its core distribution area. Therefore, as for any organism, biotic and abiotic factors will play a role in imposing its distribution range limits. The distribution of this species appears to follow biogeographic patterns operating at an ecosystem level. In the northern limit, biotic factors such as species higher diversity seem to affect Z. brevirostris distribution, whereas, in the southern border, abiotic factors such as water temperature seem to play a role in imposing its limits.
Northernmost range limit
Previous reports of Z. brevirostris further north than Espírito Santo State should be viewed with caution. The mention of Ilha Rasa for the Fernando de Noronha Archipelago (Castello, 1971 ; followed by Batista, 1987a , 1987b and Santos et al., 2006 , but not in Soto, 2001 ) is doubtful and should be disregarded. This mistake is possibly due to a misinterpretation of Miranda-Ribeiro’s ( 1904 ) records of Z. brevirostris for Ilha Rasa, Guanabara Bay, Rio de Janeiro State. Mentions of Z. brevirostris for the coastal region of Bahia State (Northeastern Brazil) lack support of museum specimens or detailed locality records. Miranda-Ribeiro ( 1907 ) mentioned Bahia State as part of this species habitat despite the absence of locality data. Other subsequent studies (Bigelow and Schroeder, 1953 , Figueiredo, 1977 , Batista, 1991 ) based their accounts on Miranda-Ribeiro ( 1907 ). This study found no additional evidence of Z. brevirostris for Bahia State. Nonetheless, Bahia and Espírito Santo States have been considered a part of an ecotone area that enables the occurrence of fauna from different subdivisions of the Brazilian Biogeographic Province (Cord et al., 2022 , Anderson et al., 2023 ). Moreover, the distribution of a species is dynamic and influenced by environmental factors associated with its life history, migration patterns, colonization, and even local extinction (Brown and Lomolino, 1998 , Luiz et al., 2012 ). It is possible that migrants of Z. brevirostris once reached southern Bahia State but fluctuations occurred temporally and the presence of this species currently remains uncertain.
Oceanographic features possibly play an important role on the northernmost range limit of Z. brevirostris . The South Equatorial Current bifurcates in Northeastern Brazil from 10°S to 15°S, generating the Brazil Current, which influences conditions in Southeastern Brazil (Peterson and Stramma, 1991 , Piola and Matano, 2019 ). The Brazil Current, along with upwellings from the south, generates a transition zone of tropical and subtropical waters in Espírito Santo State (Schmid et al., 1995 , Floeter et al., 2001 , 2007 ). Moreover, freshwater discharge from the São Francisco River (Pinheiro et al., 2018 ) and the Abrolhos Archipelago, which is characterized as a topographic barrier to the Brazil Current (Schmid et al., 1995 ), possibly influence oceanographic conditions to the north of Espírito Santo along the southeast shelf. It is already known that variations in environmental conditions strongly affect reef fish species occurrence in the area (Pinheiro et al., 2018 ). These environmental features have established Espírito Santo State as the northernmost range limit for some species (Floeter et al., 2001 , Barroso et al., 2016 , Pinheiro et al., 2018 ). Besides Z. brevirostris (Pinheiro et al., 2015 ), examples of other elasmobranches that have Espírito Santo State as their northern range limit include the Brazilian Guitarfish, P. horkelii , the Groovebelly Stingray, Dasyatis hypostigma Santos and Carvalho, 2004, and the Angular Angel Shark, Squatina guggenheim Marini, 1936 (Last et al., 2016 , Pinheiro et al., 2015 , 2018 ).
The northernmost range limit of Z. brevirostris is in a tropical area and may also be affected by biotic factors. In the tropics, biotic conditions may be drivers capable of limiting the abundance and distribution of species (Dobzhansky, 1950 , MacArthur et al., 1972 ). Commonly, these areas have a higher species richness (Brown and Lomolino, 1998 ), which might be the case for the northern range limit of Z. brevirostris since other authors (Pinheiro et al., 2018 ) have suggested a relatively high reef fish species richness.
Southernmost range limit
The southernmost range limit of Z. brevirostris is most often set as the continental shelf off Mar del Plata, in northeastern coast of Argentina (Castello, 1971 , Last et al., 2016 , Menni and Stehmann, 2000 , Santos et al., 2006 , Gomes et al., 2019 ). However, records further south in Argentina have also been mentioned, such as Puerto Quequén (Tamini et al., 2006 , Chiaramonte et al., 2011 , Barbini and Cousseau, 2015 ; see also MACN-Ict 9664) and the Gulf of San Matias (Pollom et al., 2020 ). The three occurrence records highlighted in this study [Chubut Province, Santa Cruz Province, and the Falkland Islands (Malvinas)] further extend the known distribution range for Z. brevirostris (more than 2,000 km further south than the Gulf of San Matias).
These occurrence records, reaching the Central Coast of Patagonia, may be facilitated by the Brazil Current, which could have its greatest influence in the region during summer months (Boschi, 1989 , Caille and Maldonado, 1993 ). Accordingly, the records for Chubut and Santa Cruz provinces both refer to warm months (December and February, respectively). In this region, several other species from temperate warm waters have been recorded at higher latitudes during summer months (e.g., the Dusky Grouper, Epinephelus marginatus , Irigoyen et al., 2005 ; the Silver Porgy, Diplodus argenteus , Galvan et al., 2005 ; the Namorado Sandperch, Pseudopercis numida , Venerus et al., 2007 ; the Spotback Skate, Atlantoraja castelnaui , the Eyespot Skate, Atlantoraja cyclophora , the Atlantic Moonfish, Selene setapinnis , the Cochero, Dules auriga , the Argentine Goatfish, Mullus argentinae , the Brazilian Codling, Urophycis brasiliensis , the Red Porgy, Pagrus pagrus and the Largehead Hairtail, Trichiurus lepturus , Góngora et al., 2009 , Bovcon et al., 2011 ; the Snowy Grouper, Hyporthodus niveatus , Trobbiani et al., 2014 ; the Tope, Galeorhinus galeus , Chiaramonte et al., 2016 ; the Striped Smoothhound, Mustelus fasciatus , and the Shortnose Eagle Ray, Myliobatis ridens , Chiaramonte et al., 2023 ).
In turn, the record of Z. brevirostris in the Falklands Islands (Malvinas) suggests a physiological plasticity for the species given the low water temperature in the region (4 to 10° C, influenced by cold waters from the Malvinas Current - Piola and Matano, 2019 ). Possibly, factors other than water temperature, such as salinity, depth, and bottom substrate type, further allow the occurrence of this species in the region. For instance, Z. brevirostris is intimately related to ocean floors that are flat and composed of sand, mud, and gravel (Barbini et al., 2011 ). All these conditions are present in the Patagonian Continental Shelf of Argentina, in which the Falklands Islands (Malvinas) are located (Violante et al., 2014 ).
Overall, biotic factors may influence the distribution of a species, affecting its range limit on one side (usually at low latitudes), whereas abiotic conditions might be the limiting factors on the other extreme of its range (usually at high latitudes) (Dobzhansky, 1950 , Brown and Lomolino, 1998 , MacArthur et al., 1972 , Paquette and Hargreaves, 2021 ). This seems to apply to Z. brevirostris , which may have its southernmost range limit affected by abiotic factors. This area is influenced by the Malvinas Current and the Brazil/Malvinas confluence (Piola and Matano, 2019 ). Environmental conditions such as bottom type, decreasing water temperature, increasing salinity, dissolved oxygen, and latitude affect the spatial distribution of many other species in this region (Menni et al., 2010 , Barbini et al., 2011 , Lucifora et al., 2012 ). Water temperature influences the geographical distribution of fish (Menni et al., 2010 , Sunday et al., 2012 , Rutterford et al., 2023 ). Water temperature (which is related to latitude) and depth are the abiotic factors that most influence (working as ecological drivers) the geographic distribution of Chondrichthyes in the Southwest Atlantic (Menni et al., 2010 ). For instance, influence of water temperature may even result in the splitting of the Chola Guitarfish, Pseudobatos percellens , into distinct genetic lineages (Cruz et al., 2023 ).
It is unknown if Z. brevirostris has established a population at its southernmost limit or if its presence in the region is due to occasional migrants. In fact, it is unclear if Z. brevirostris completes its life cycle throughout its entire geographic distribution range. Movements of Chondrichthyes further south of their distribution are mostly considered to be occasional or seasonal in the Southwestern Atlantic (Menni et al., 2010 ). This may explain a relatively sparser occurrence of Z. brevirostris at its southernmost limit when compared to its northernmost limit.
ACKNOWLEDGMENTS
L.G.X. is thankful to M. Stehmann (ICHTHYS), R. Thiel and I. Eidus (ZMH), E. V. Silva and M. R. Britto (MNRJ), R. Robins (FLMNH), R. de Ruiter (RMNH), B. Brown (AMNH), P. Bartsch (ZMB), J. Williams (USNM), G. Chiaramonte (MACN), A. Gosztonyi (CENPAT), S. Barbini (INIDEP), E. Giácomo (IBMPAS), and M. Loureiro (MHNM) for museum specimen information. L.G.X. and V.V.F. are also thankful to J. González (MHNM), J. Astarloa (UNMdP), M. Estalles (CONICET), C. Sampaio (UFAL), C. Ferreira (UFF), S. Floeter (UFSC), and J. Santander-Neto (IFES) for information on Z. brevirostris occurrence. CAPES provided a PhD fellowship to L.G.X. and a postdoctoral fellowship (Programa Nacional de Pós-Doutorado - PNPD) to J.E.P.F. FUNCAP provided a visiting researcher grant to P.C. We are thankful for the comments provided by two anonymous reviewers, which improved the manuscript.
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