Abundance dynamics of a new, endemic batoid from Brazil: The Lutz’s stingray, Hypanus berthalutzae

https://doi.org/10.1016/j.rsma.2021.102059Get rights and content

Abstract

The Lutz’s stingray, Hypanus berthalutzae, is a recently identified, endemic dasyatid species which occurs in shallow habitats exclusively along most of the Brazilian coast. It is frequently caught as bycatch in different fisheries throughout the range of its distribution, but information on population trends and the impacts of fishing is still scarce. Therefore, this study aimed to describe the structure and dynamics in H. berthalutzae relative abundance off Recife, Northeast Brazil, in order to provide baseline data for species management. H. berthalutzae were caught and sampled in a fisheries-independent, standardized longline and drumline survey which used > 500,000 hooks during 11 years. H. berthalutzae catch composition (N = 86) was characterized by a striking predominance of females, with a female:male ratio of 16:1. Most of these individuals measured were considered to be mature. H. berthalutzae catch rates were largely reduced after hooks previously operating directly on the seafloor were suspended in the middle of the water column. Such an effect was included in a zero-inflated generalized additive model developed to assess spatiotemporal and environmental modulators of H. berthalutzae abundance, for which both month and lunar phase proved to be statistically significant predictors. A higher abundance of H. berthalutzae was observed in the rainy season, from March to July (χ2= 19.22; p < 0.001), as well as during full moon periods (Z = 2.38; p = 0.017). The effects of other candidate predictors such as sampling site or year were either nonexistent or superimposed by other more deterministic factors. The results achieved in this fully standardized survey depict the dynamics in adult H. berthalutzae which might be expected to occur in coastal habitats off northeastern Brazil, thus providing a solid contribution to improve the management of local artisanal fisheries towards the recovery and sustainability of H. berthalutzae populations across their range.

Introduction

Elasmobranchs generally have low fecundity, large body sizes, slow growth rates, late sexual maturity, and long lifespans (Garcia et al., 2007). These life history traits endow elasmobranchs with a low reproductive potential and limited capacity to recover from population disturbance (Stevens et al., 2000). In addition, as elasmobranchs generally are high-level consumers (Camhi et al., 1998), their abundance is typically low (Stevens et al., 2000, Walker, 1998). Such aspects, coupled with the rapid degradation of coastal ecosystems and an intensification of fishing pressure, are responsible for threatening the sustainability of many elasmobranch populations globally (Jackson et al., 2001, Smith et al., 2008, Dulvy et al., 2014), inclusively in the South Atlantic Ocean (Gonçalves-Silva and Vianna, 2018, Rodrigues et al., 2019).

Although sharks and rays have been historically exploited by several fisheries as bycatch, some species have become targeted in recent decades (Baum et al., 2003, Barreto et al., 2016). In Brazil, data on oceanic sharks caught primarily by the industrial tuna longline fishery are available to a great extent due to commitments of the country as a member of the International Commission for the Conservation of Atlantic Tunas (ICCAT). On the other hand, fisheries information is much scantier for coastal elasmobranchs as these are mostly caught by artisanal fisheries operating along the entire Brazilian coast (Bornatowski et al., 2017). When landing data are available for such fisheries, elasmobranchs are usually reported simply as “sharks” or “rays” (Barreto et al., 2017), thus precluding the ability to conduct species-specific assessments and management.

The global fishing production of Chondrichthyes (i.e., elasmobranchs and chimaeras) as reported by the Food and Agriculture Organization (FAO) was estimated at about 760,000 tons, of which 30% corresponded to batoids (i.e., rays and skates) (FAO, 2014). However, these data do not reflect real fishing mortality rates as they do not include discards and/or unreported catches. In fact, the actual fishing mortality rates of these taxa are likely to be about 3 to 4 times greater than those officially reported (Dulvy et al., 2014). Worldwide, batoids are frequently targeted or caught as bycatch in several fisheries including trawling, gillnetting, and longlining (Last et al., 2016). In Brazil, the annual average batoid catch by the fishing industry has been estimated at 5000 tons (Marceniuk et al., 2019). Yet, and despite some species enduring heavy exploitation rates, information on batoid catch rates has been historically absent from national fisheries statistics (Bornatowski et al., 2017). As with sharks, a lack of species identification on batoid landing data preclude the assessment of species-specific fishing mortality rates and, subsequently, the development of effective conservation and management measures (Bornatowski et al., 2017, Santander-Neto and Faria, 2020).

Although more than 600 batoid species have been identified (Kriwet et al., 2009, Last et al., 2016), this group has been much less studied than sharks, probably due to high discard rates at sea and the underreporting of their catches (Ebert and Cowley, 2003, Freitas et al., 2019). Consequently, serious depletions in batoid populations may be undergoing completely unnoticed. A clear symptom of this is the lack of comprehensive assessments of the conservation status in batoids, with 20.3% of these species being listed as Data Deficient (IUCN, 2021). Furthermore, those taxa for which more information is available seem to endure worrying amounts of threat. Among dasyatid stingrays, for instance, 24.1% of the species are listed as Endangered (EN), 29.1% as Vulnerable (VU), and 15.2% as Data Deficient (IUCN, 2021). Such a scenario strongly demonstrates the urgency in implementing effective management measures that can successfully ensure the sustainability of stingray populations. However, this goal is often hampered by a lack of proper knowledge about the biological specificities of each individual taxon subject to anthropic pressure, which is not surprising since the phylogeny of many marine species is yet to be thoroughly understood.

As a matter of fact, a new dasyatid stingray species, the Lutz’s stingray, previously believed to correspond to Hypanus americanus has been recently described off the coast of Brazil. The identification of this new species was based on an integrative approach combining genetics, morphology and ecological niche modeling which demonstrated that the differentiation between the new species and three other closely related species from the Hypanus genus (i.e., H. americanus, H. longus, and H. rudis) was significant, with the height and length of the ventral caudal fold and both interspiracular and interorbital lengths being useful measurements to distinguish the four species (Petean et al., 2020). This seemingly endemic species has been named Hypanus berthalutzae sp. nov. (Petean et al., 2020) and its speciation may have occurred due to the great discharge of freshwater and sediments into the ocean by the Amazon River, which likely acted as a barrier for stingray dispersion across the continental platform (Petean et al., 2020). Notwithstanding, H. berthalutzae seems to share many bioecological traits with H. americanus and all the previous knowledge gathered about the latter could be at least partially applied to the former. Despite its most recent identification, population assessments indicate that H. berthalutzae is presently vulnerable to extinction as per IUCN criteria (Charvet et al., 2020), which is in line with the current classification of H. americanus as near threatened (Carlson et al., 2020).

H. berthalutzae is a demersal, large-bodied, coastal stingray occurring from the Amazon River mouth through Southeast Brazil (Costa and Chaves, 2006, Meneses et al., 2006, Yokota and Lessa, 2006, Torres et al., 2007), including remote oceanic islands such as the Archipelago of Fernando de Noronha and the Rocas Atoll (Aguiar et al., 2009, Branco-Nunes et al., 2016). Although H. berthalutzae is frequently caught as a bycatch in different Brazilian fisheries, most notably in trawling, there is still little information available on population trends and the possible impacts of fishing throughout its distribution range (Charvet et al., 2020). H. berthalutzae incidental catch in trammel nets, bottom trawls and bottom longlines by artisanal fisheries has increased considerably in some regions of Brazil, for instance, raising concerns about the sustainability of their exploitation (Meneses et al., 2006, Yokota and Lessa, 2006, Torres et al., 2007, Tagliafico et al., 2013, Santander-Neto and Faria, 2020). Increasing the knowledge about the vulnerabilities of H. berthalutzae is of outmost importance and previous research focused on this species and on the closely-related H. americanus addressed several aspects including habitat use and aggregations patterns (Aguiar et al., 2009, Tilley and Strindberg, 2013, Vaudo et al., 2017), reproduction (Henningsen, 2000, Silva et al., 2007, Ramírez-Mosqueda et al., 2012), mating behavior (Chapman et al., 2003), and feeding strategies (Gilliam and Sullivan, 1993, Corcoran et al., 2013). However, few studies have yet assessed the dynamics in stingray abundance and distribution, with most of the information available being restricted to the Caribbean Sea (Gilliam and Sullivan, 1993, Tilley and Strindberg, 2013, Corcoran et al., 2013, Briones et al., 2017).

In this context, this study aimed at describing the population structure of H. berthalutzae and at examining trends in their abundance in coastal habitats off northeastern Brazil across spatial, temporal, and environmental scales. We expect such an information to provide a solid contribution to marine and conservation sciences by ascertaining some ecological aspects and vulnerabilities of this little-known stingray species to fishing pressure, which is utterly required for managing purposes since H. berthalutzae distribution makes it readily accessible to a plethora of fishing practices.

Section snippets

Ethics statement

This study was conducted with the approval of the Instituto Chico Mendes de Conservação da Biodiversidade of the Brazilian Ministry of the Environment (permit no. 15083-8). The capture and handling of rays was approved and carried out in full compliance with the recommendations of the Commission of Ethics on the Usage of Animals of the Federal Rural University of Pernambuco (license no. 041/2009).

Study area

This study was conducted off a 20-km stretch of coastline in the Metropolitan Region of Recife

Fishing effort and catch composition

Overall, fishing effort comprised 505,861 hooks distributed in 3470 longline and 6907 drumline fishing sets, which were conducted in 413 fishing trips. There was some variability in the yearly amount of fishing effort during the study period, with 2006 and 2010 being the years when the largest numbers (36,000–37,000) of hooks were deployed (Fig. 2).

A total of 86 H. berthalutzae were caught, with 98% being delivered by longline gear. Only two specimens, more precisely two females measuring 121

Discussion

Achieving a proper understanding of species distribution across spatiotemporal and environmental scales is an unavoidable priority when designing effective resource management strategies (Peterson and Grubbs, 2020, Santander-Neto and Faria, 2020). In Brazil, however, knowledge about batoid distribution and abundance trends is extremely scarce, making the assessment of their population status difficult to assess. Hypannus guttatus and H. berthalutzae are among the most commonly landed ray

Conclusions

The results herein introduced indicate that potential management measures including changes in gear configuration and time–areaclosures could be very efficient in reducing H. berthalutzae fishing mortality. Further research is yet warranted to thoroughly understand the spatiotemporal dynamics in H. berthalutzae abundance across its whole distribution, but the amount of knowledge so far gathered about this and other dasyatid species should be used to shape ecologically-based management measures

CRediT authorship contribution statement

Ilka Branco-Nunes: Conceptualization (supporting), Investigation (lead), Visualization (lead), Methodology (supporting), Writing – original draft (lead), Writing – review & editing (lead). Yuri Niella: Formal analysis, Writing – original draft (supporting). Fábio Hissa Vieira Hazin: Visualization (supporting), Supervision, Project administration, Funding acquisition, Writing – review & editing (supporting). Emmanuelly Creio: Methodology (supporting), Investigation (supporting). Paulo Guilherme

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

The authors are thankful to the crew of R.V. Sinuelo and R.V. Pedrinho and to all interns from the Laboratório de Tecnologia Pesqueira at the Universidade Federal Rural de Pernambuco (LATEP/UFRPE) for assisting with field work. This work was funded by the State Government of Pernambuco, Brazil. IBN sincerely thanks FACEPE - Fundação de Amparo a Ciência e Tecnologia do Estado de Pernambuco for her PhD and postdoctoral fellowship. Funding to YN through an International Macquarie University

References (65)

  • BaumJ.K. et al.

    Collapse and conservation of shark populations in the Northwest Atlantic

    Sci.

    (2003)
  • BornatowskiH. et al.

    Elasmobranchs consumption in Brazil: impacts and consequences

  • Branco-NunesI.S.L.

    Ecologia Da Raia, Dasyatis Americana (Hildebrand & Schroeder, 1928), Na Região Metropolitana do Recife - PE e na ReBio Atol das Rocas – Brasil, Brazil

    (2015)
  • Branco-NunesI. et al.

    Vertical movements of the southern stingray, Dasyatis americana (Hildebrand and Schroeder, 1928) in the Biological Reserve of the Rocas Atoll, Brazil

    Lat. Am. J. Aquat. Res.

    (2016)
  • BrionesA. et al.

    Captura incidental de la raya Hypanus americanus (Elasmobranchii) en la pesca de arrastre de camarón en la región suroriental de Cuba

    Lat. Am. J. Aquat. Res.

    (2017)
  • CamhiM. et al.

    Sharks and their Relatives, Ecology and Conservation

    (1998)
  • CarlsonJ. et al.

    Ginglymostoma cirratum

  • CarlsonJ. et al.

    Hypanus americanus

  • ChapmanD.D. et al.

    Mating behavior of southern stingrays, Dasyatis americana (Dasyatidae)

    Environ. Biol. Fish.

    (2003)
  • CharvetP. et al.

    Hypanus berthalutzae

  • CorcoranM.J. et al.

    Supplemental feeding for ecotourism reverses diel activity and alters movement patterns and spatial distribution of the southern stingray, dasyatis americana

    PLos One

    (2013)
  • CostaL. et al.

    Elasmobrânquios capturados pela pesca artesanal na costa sul do Paraná e norte de Santa Catarina, Brasil

    Biota Neotrop.

    (2006)
  • DulvyN.K. et al.

    Extinction risk and conservation of the world’s sharks and rays

    Elife

    (2014)
  • EbertD.A. et al.

    Diet, feeding and habitat utilization of the blue stingray Dasyatis chrysonota (Smith, 1828) in South African waters

    Mar. Freshw. Res.

    (2003)
  • Eskinazi-LeçaE. et al.

    Oceanografia: Um Cenário Tropical

    (2004)
  • The State of World Fisheries and Aquaculture

    (2014)
  • FerreiraL.C. et al.

    Habitat use of the nurse shark, Ginglymostoma cirratum, off Recife, Northeast Brazil: a combined survey with longline and acoustic telemetry

    Environ. Biol. Fish.

    (2012)
  • FreitasR.H.A. et al.

    Unravelling the foraging behavior of the southern stingray, Hypanus americanus (Myliobatiformes: Dasyatidae) in a Southwestern Atlantic MPA

    Neotrop. Ichthyol.

    (2019)
  • GarciaV.B. et al.

    The importance of habitat and life history to extinction risk in sharks, skates, rays and chimaeras

    Proc. R. Soc. B: Biol. Sci.

    (2007)
  • GilliamD. et al.

    Diet and feeding habits of the southern stingray Dasyatis americana in the Central Bahamas

    Bull. Mar. Sci.

    (1993)
  • Gonçalves-SilvaF. et al.

    Use of a species-rich and degraded tropical estuary by Elasmobranchs

    Braz. J. Oceanogr.

    (2018)
  • HazinF.H.V. et al.

    A green strategy for shark attack mitigation off Recife, Brazil

    Animal Conserv.

    (2013)
  • Cited by (4)

    View full text