Chondrichthyan fauna from the Marine Protected Area Namuncurá at Burdwood Bank: exploring egg nursery grounds

doi:10.21203/rs.3.rs-2247873/v1

Download PDF

Research Article

Chondrichthyan fauna from the Marine Protected Area Namuncurá at Burdwood Bank: exploring egg nursery grounds

https://doi.org/10.21203/rs.3.rs-2247873/v1

This work is licensed under a CC BY 4.0 License

Journal Publication

published 08 Apr, 2023

Read the published version in Polar Biology →

You are reading this latest preprint version

The Burdwood Bank (BB) is a subantarctic area, where two of the three Marine Protected Areas (MPA) of the Argentinean Exclusive Economic Zone are located: Namuncurá I, and Namuncurá II. The area is characterized by a high biodiversity of benthic invertebrates and teleost fishes; however, the available information on oviparous chondrichthyans is scarce. The aim of this study is to explore the potential reproductive use that oviparous chondrichthyans could make of the area based on the presence of egg-laying grounds. Additionally, we aim to provide an updated checklist of the species that inhabit the BB. Samples of specimens and egg capsules collected in four research cruises carried out between 2016 and 2018 were analyzed. Seven skate species were found in both MPAs: Amblyraja doellojuradoi, Bathyraja albomaculata, B. brachyurops, B. macloviana, B. multispinis, B. scaphiops, and Psammobatis rudis; whereas B. cousseauae, and B. magellanica were found exclusively in Namuncurá I. Here we report, for the first time, the presence of egg laying grounds for five chondrichthyan species in the BB area: A. doellojuradoi, B. brachyurops, B. macloviana, B. scaphiops, and P. rudis. The results obtained highlighted the importance of the region for the conservation of oviparous chondrichthyans found in the southern Patagonian shelf.

MPAs

egg-laying

skates

Southwest Atlantic

Chondrichthyans are thought to play key ecological roles within the marine ecosystem (Heithaus et al. 2010; Costa et al. 2015; Roff et al. 2016). They occupy medium-to-high trophic levels and are also prey of larger predators (Dean et al. 2017, Navia et al. 2017), providing the connection between higher and lower levels (Vaudo and Heithaus 2011), and influencing the stability and robustness of the ecosystem (Dunne et al. 2004). They can determine species replacement and control the populations of other predators (Martins et al. 2018; Stevens et al. 2000). Additionally, some species can travel large distances between habitats (Collins et al. 2007, 2008), thus linking trophic webs and enhancing nutrient exchange (Sheaves 2009). Finally, due to their feeding behaviors, benthic chondricthyans favor bioturbation, which has a beneficial impact on benthic fauna (Martins et al. 2018).

The wide evolutionary success of chondrichthyans may be attributed to their diversity of reproductive strategies (Musick and Ellis, 2005). Oviparity is a well-represented reproductive mode found in all skates (Rajiformes), and some species of sharks (some Carcharhiniformes, Heterodontiformes, and Orectolobiformes), and holocephalans (Chimaeriformes) (Nakaya et al. 2020), and is based on the release of egg capsules on the sea bottom. The embryonic development occurs inside the egg capsules and the incubation periods range from a few months to several years (Berestovskii 1994; Hamlett and Koob 1999; Jañez and Sueiro 2007; Mabragaña et al. 2015; Vazquez 2020). Females usually lay their eggs in specific sites known as nursery areas (Love et al. 2008), where the availability of food and the lower predation risk are some of the most important features (Martins et al. 2018). The structure of the bottom and the diversity of benthic organisms can also be essential in determining nursery areas; these areas have been found over soft sea floors (Lucifora and García 2004; Hoff 2007) and over rocky areas (Love et al. 2008; Hunt et al. 2011; Treude et al. 2011), and there is also evidence of associations between egg capsules and benthic invertebrates (Ellis et al. 2005; Treude et al. 2011; Henry et al. 2013; Vazquez et al. 2018). The identification of a site as a nursery area is made following four criteria established by Hoff (2006), however, when some of these criteria are not fulfilled, the term egg-laying grounds is more suitable to refer to these areas (Martins et al. 2018).

Chondrichthyans catches have increased considerably both globally (Stevens et al. 2000), and regionally (Sánchez 2010) in the last decades. Approximately, one-third of chondrichthyan species worldwide are estimated to be threatened, being overfishing the principal cause of threat, followed by loss and degradation of habitat, climate change, and pollution (Dulvy et al. 2021). In the Southwest Atlantic (SWA) Ocean, the situation is not much different; drastic decreases of chondrichthyan populations have been registered, particularly in the Argentinean Sea (Massa et al. 2004). The shelf and slope of this area are inhabited by c.a 35 species of oviparous chondrichthyans, including 32 skates, one holocephalan, and two sharks (Menni and Stehmann 2000; Cousseau et al. 2007; Gabbanelli et al. 2018; Cousseau et al. 2020; Sabadin et al. 2020; Weigmann et al., in press). Approximately half of these species were registered in the Atlantic sector corresponding to the Magellanic and the Patagonian Slope Provinces (Menni and Stehmann 2000; Arkipkhin et al. 2012; Cousseau et al. 2020; Sabadin et al. 2020). The implementation of fishing regulations, sanctuaries, and Marine Protected Areas (MPAs) is fundamental for the conservation of threatened taxa, such as chondrichthyans. MPAs play a key role in the feeding, development, reproduction, sheltering, and management of these populations (Becerril-García et al. 2022). Additionally, the proper management and performance of MPAs can help ameliorate the drastic consequences of climate change, helping to safeguard critical ecological processes, reducing biodiversity losses and decreasing anthropological stressors, among others (Roberts et al. 2017).

There are only three oceanic MPAs recently created in the Argentinean Exclusive Economic Zone: “Namuncurá-Banco Burdwood I”, “Namuncurá-Banco Burdwood II” (which incorporates the southern slope area) located at Burdwood Bank (BB) area, and Yaganes. The BB is a 28,000 km²-subantarctic area located between 53°30′ S-55° S and 55° W-62° W, consisting of an underwater plateau ranging from 50 to 200 m depth, where it breaks into a wall reaching 1100–3000 m depths (Zunino and Ichazo 1979). This plateau presents a highly heterogeneous bottom surface, with patches of rocky areas and others dominated by coarse biogenic sand; whereas the shelf-break is characterized by a rocky slope dominated by cold-water coral reefs (Schejter et al. 2016, 2017). The hard bottoms show a higher diversity of benthic invertebrates (Schejter et al. 2017) and fishes (Delpiani et al. 2020) than the soft bottoms. The BB harbors more than 240 taxa of benthic organisms (Schejter et al. 2016), and close to 10% of the fish composition reported for the Atlantic sector of the Magellanic Province (Delpiani et al. 2020, Cousseau et al. 2020). Numerous species of benthic invertebrates have been found in the BB, including some vulnerable and endemic species (Falabella et al. 2017). These organisms have an essential role in marine ecosystems (Allega et al. 2020), due to their ability to structure the bottom surface providing new niches, thus creating new habitats for other species (Bremec et al. 2017). Additionally, the BB is found within a marine front, which leads to high primary production and therefore high availability of food (Falabella et al. 2017).

In the Argentinean Sea, egg-laying grounds have been recognized for some skate species associated with marine fronts at the continental shelf and slope (Vazquez et al. 2016). A lot of research about the reproductive biology of chondrichthyans that inhabits southern Patagonia is also available (Mabragaña and Cousseau 2004; Ruocco et al. 2006; Cousseau et al. 2007; Arkhipkin et al. 2008; Mabragaña et al. 2011; Scenna 2011; Arkhipkin et al. 2012; Scenna and Díaz de Astarloa 2014; Delpiani 2016), but studies determining if reproductive events are taking place at BB are lacking. Considering the richness and abundance of benthic organisms in the area (Schejter et al. 2016, 2017, 2020), the complex structure of the sea bottom, the association between egg capsules and benthic organisms found in neighboring areas (Vazquez et al. 2018), and the food availability (Covatti et al. 2022, Fischer et al. 2022), the BB could be a suitable habitat for chondrichthyan egg-laying. Therefore, the aim of this study is to explore the potential reproductive use that oviparous chondrichthyans could make of the area based on the presence of egg-laying grounds. Additionally, we provide an updated checklist of chondrichthyan oviparous species that inhabit the BB.

Sample collection

Collection of both specimens and egg capsules was carried out in the south portion of the Southwest Atlantic between 53º25´53.7´´ − 55º6´27.42´´ S and 58º − 68º29´35.52´´ W from 33 m to 785 m depth. Samples came from four research cruises: three on board of the Argentinean O/V “Puerto Deseado” between 2016 and 2018, and one on board of the R/V “Víctor Angelescu” in 2018. Three bottom trawls were used to collect samples: a small net (50 mm mesh in the wings, and 20 mm in the cod end; horizontal opening 6 m), a big net (135 mm mesh in the wings, and 60 mm in the cod end; horizontal opening 16 m), and an Engel-type net (200 mm mesh in the wings, and 103 mm in the cod end; horizontal opening 35.3 m). Tow duration was between 5 and 20 minutes and the trawling speed was from 1.5 and 5 knots. A total of 110 hauls were carried out taking into account all cruises; 65 were placed at the plateau and slope of BB (Fig. 1A). For each haul, date, latitude, longitude, and depth were recorded (Online Resource 1). The cruises were not designed to study chondrichthyans exclusively, therefore the most used trawl (small net) was not the target for collecting large specimens.

The sampling area was divided into four smaller areas: Namuncurá I, Namuncurá II, the northwest slope of Namuncurá I (NW Slope), and the Comparative Area (CA) that includes all the hauls performed outside of the BB (Fig. 1B). The first two areas correspond to the current MPAs. We decided to study the NW Slope separately due to the high biodiversity and fragile ecosystems that harbors (Schejter and Bremec 2019).

Sample identification

Samples were collected, measured, and frozen on board for subsequent examination in the laboratory. The specimens were identified following Cousseau et al. (2007) and Figueroa (2011), whereas egg capsules were identified following Mabragaña et al. (2011, 2017). Total length (TL), and maximum width of the disc (DW) for skates or maximum width (MW) for sharks were recorded, whereas length (excluding horns) (ECL) and maximum width (MAW) were registered for egg capsules. Samples were fixed in 4% formalin and stored in 70% alcohol at the ichthyological collection of Instituto de Investigaciones Marinas y Costeras (Universidad Nacional de Mar del Plata, Argentina).

Occurrence, richness, and abundance patterns

Specimens or egg capsules occurrence for each species was recorded and discriminated for area to update the oviparous chondrichthyan species present at the BB. The number of egg capsules per haul was recorded for each species. Data from all cruises and all types of nets were considered in order to describe both species occurrence and richness patterns. Abundance estimations were made only for egg capsules, due to the small number of specimens collected. Only hauls coming from the small net were considered to avoid errors due to net differences. The relative abundance (or density) of egg capsules was estimated by the swept area method (Alverson and Pereyra 1969), expressed as capsules per km². The swept area was calculated as s x t x ha, where s is the trawling speed (km/h), t is the duration of trawling (h) and ha is the horizontal opening of the trawl (km). The horizontal aperture was corrected as 70% of the headline length (6m) following Okonski & Martini (1987). This correction resulted in a ha of 4.2 m. The relative abundance was calculated for all species taken together and for each individual species, and was used as an indicator of possible egg-laying grounds, being those hauls with maximum density or high densities of particular interest. All maps were produced using Surfer. 10.

Embryonic development

All captured closed egg capsules were examined for embryo presence. Embryo total length (TL), maximum width of the disc (DW) or maximum width (MW), and external yolk-sac diameter (EYS) were measured. The embryo stage was determined following Brant (2006) for skates, and Ballard et al. (1993) for sharks. These studies considered a total of 35 and 34 stages respectively based on external and internal morphology. Embryos were grouped into initial (< 17), early (18 to 24), middle or intermediate (25 to 29), advanced (30 to 34) and pre-hatching (35) following Vazquez (2020), to make inferences on potential egg-laying seasons, when possible.

Specimen occurrence patterns

A total of 110 hauls were carried out in the whole area, from which 26.4% were positive for specimens (Fig. 2A). A total of 65 specimens of 11 species of oviparous chondrichthyans were collected, including 10 skates and one shark (Table 1). Specifically in the BB, specimens of 9 skate species from genus Amblyraja, Bathyraja and Psammobatis were found (Table 1). All the specimens were identified to species level except one individual found at Namuncurá I, which was assigned to the genus Bathyraja. It corresponded with a female specimen caught at 140 m depth (TL = 337 mm; DW = 243 mm). Bathyraja cousseauae, and Psammobatis rudis were registered for the first time at BB (Table 1). Specimens of B. cousseauae were found at Namuncurá I at 177 m depth; whereas those of P. rudis were found in both Namuncurá I at 128 m and Namuncurá II at 422 m. Females bearing egg capsules were not found at BB. One female of S. bivius (TL = 545 mm) carrying egg capsules was found in the Beagle Channel at 233 m depth, and one of B. cousseauae (TL = 1210 mm) near Isla de los Estados at 293 m.

Table 1

Checklist of oviparous chondrichthyans found at the surveyed area. The number of specimens or egg capsules found in each area is indicated. CA: comparative area, N-I: Namuncurá I, N-II: Namuncurá II, NW S: Northwest slope. N-I, N-II, and NW S are found within the Burdwood Bank area, whereas the comparative area is found in the southern Patagonian shelf.
	Specimens				Egg capsules
	N-I	N-II	NW S	CA	N-I	N-II	NW S	CA
Amblyraja doellojuradoi	1	5	3				16
Bathyraja albomaculata	8	5		1
Bathyraja brachyurops	4	1			25	1		2
Bathyraja cousseauae	1			6				2
Bathyraja macloviana	9				6	24		6
Bathyraja magellanica	1			2	1			16
Bathyraja multispinis		2
Bathyraja scaphiops	1				3	8		4
Bathyraja sp.	1
Psammobatis normani								10
Psammobatis rudis	1	1		2	1			17
Schroederichthys bivius				8				36
Zearaja brevicaudata				1

Egg capsule occurrence patterns

Forty-nine percent of hauls were positive for egg capsules in the whole area (Fig. 2B). A total of 199 egg capsules of 9 species were collected, including one shark and eight skates (Table 1). Specifically in the BB, egg capsules of six species of skates (A. doellojuradoi, B. brachyurops, B. macloviana, B. magellanica, B. scaphiops, and P. rudis) (Table 1) were found for the first time in the area. Egg capsules were found in both Namuncurá I and II, and also in NW Slope (Fig. 2B). The frequency of occurrence of egg capsules at BB was: B. brachyurops (29.2%); B. macloviana (24.6%); P. rudis (7.69%); A. doellojuradoi (4.6%); B. scaphiops (4.6%); and B. magellanica (1.5%).

Within the family Rajidae (hardnose skates), egg capsules of A. doellojuradoi were recovered only from the NW Slope between 209 and 642 m depth (Fig. 3A). Within the family Arhynchobatidae (softnose skates), egg capsules of Bathyraja and Psammobatis genus were found. Most of the egg capsules of B. brachyurops were found at BB, between 81 and 608 m depth in both Namuncurá I and Namuncurá II (Fig. 3B). Egg capsules of B. cousseauae were captured exclusively at the CA at 263 m (Fig. 3C). Egg capsules of B. macloviana were recovered in all the regions sampled between 78 and 785 m depth except in the NW Slope (Fig. 3D); most of the egg capsules of this species were found at Namuncurá I. Most of the egg capsules of B. magellanica were found at the CA between 71 and 118 m (Fig. 3E), and only one capsule was recovered from Namuncurá I at 97 m depth. The majority of B. scaphiops egg capsules were found at Namuncurá II between 694 and 785 m depth (Fig. 3F); records from the CA at 263 and 516 m were also collected. On the other hand, within the genus Psammobatis, egg capsules of P. normani were found exclusively at the CA (Beagle Channel and waters near Tierra del Fuego) between 40 and 114 m (Fig. 3G), not being present at BB. Egg capsules of P. rudis were recovered at Namuncurá I between 101 and 140 m depth and at the CA between 43 and 681 m (Fig. 3H). Finally, within the family Scyliorhinidae, egg capsules of S. bivius were recovered only at the CA between 71 and 119 m depth (Fig. 3I).

Egg capsule richness and abundance patterns

Egg capsule richness ranged from one up to four species per haul (Fig. 4A). A 57.4% of the hauls were monospecific, 27.8% were composed of two species, 13% of three, and only one haul recovered four species. The BB showed a maximum richness of three species per haul.

General egg capsule abundance (all species taken together) ranged from 40 to 4322 capsules/km², with the highest value found at the NW Slope (Fig. 4B). The maximum and minimum densities per species in each area are shown in Table 2. The maximum density for A. doellojuradoi (4322 egg capsules/km²) was the highest value observed for any species, and it was located at the NW Slope at 642 m depth (Fig. 5A). The highest density for B. brachyurops (2411 egg capsules/km²; Fig. 5B), and B. macloviana (1671 egg capsules/km²; Fig. 5C) were found at Namuncurá I at 98 m and 124 m depths, respectively. High densities of B. macloviana were also detected at Namuncurá II. Egg capsules of B. cousseauae were exclusively recorded in one haul near Isla de los Estados at 263 m depths, with a density of 558 egg capsules/km². The highest density of B. magellanica (1102 egg capsules/km²; Fig. 5D) was found at the CA at 71 m depth. The highest densities of B. scaphiops (1446 egg capsules/km²) were registered at Namuncurá II in two hauls at 785 m and 694 m depth (Fig. 5E). The highest density for P. normani (2314 egg capsules/km2) was located in the Beagle Channel at 71 m depth (Fig. 5F). On the other hand, although the highest density for P. rudis was observed at the CA (838 egg capsules/km²), a close density value was found at Namuncurá I (789 egg capsules/km²) at 140 m depth (Fig. 5G). Finally, the highest density of S. bivius (1337 egg capsules/km²; Fig. 5H) was recorded at the CA and 78 m depth.

Table 2

Egg capsule abundance found at the surveyed area. The minimum and maximum densities found in each area are shown.
	Whole Area	CA	NW Slope	Namuncurá II	Namuncurá I
Amblyraja doellojuradoi	296-4322^a	-	296–4322	-	-
Bathyraja brachyurops	257–2411 ^a	-	-	-	257–2411
B. cousseauae	532	532	-	-	-
B. macloviana	40-1671 ^a	116–571	-	1446	40-1671
B. magellanica	53-1102	53-1102	-	-	514
B. scaphiops	254–1446 ^a	254–798	-	1446	-
Psammobatis normani	532–2204	532–2204	-	-	-
P. rudis	116–798	116–798	-	-	278–760
Schroederichthys bivius	282–1483	282–1483	-	-	-
^a Maximum density found within the Burdwood Bank area.

Embryonic development

Eighteen embryos at different development stages of six species were found (Table 3). An intermediate stage embryo of B. brachyurops was captured in August. Two initial, and one advanced embryos of B. macloviana were captured in March/April, and August, respectively. Two advanced, and one pre-hatching embryos of B. magellanica were captured in November. An advanced embryo of B. scaphiops was captured in April. An initial embryo of P. rudis was taken in August. Finally, one initial, two intermediate, and six advanced embryos of S. bivius were caught in November.

Table 3

Embryo stages found. Skate embryonic stages were determined following Brant (2006), whereas Ballard et al. (1993) was used for sharks. Capture date, embryo total length (TL), disc width (DW) or maximum width (MW), and external yolk-sac diameter (EYS) are also shown.
	Skate embryonic stages	Shark embryonic stages	Capture date	TL (mm)	DW (mm)	MW (mm)	EYS (mm)
Bathyraja brachyurops	27/28		August	47.07	8.28		46.07
Bathyraja macloviana	< 17		March
	< 17		April
	31		August	79.75	22.97
Bathyraja magellanica	30		November	48.83	13.24		36.69
	33		November	94.85	32.67		43.12
	35		November	116.92	53.92		39.67
Bathyraja scaphiops	32/33		April	81.29	26.2
Psammobatis rudis	< 17		August
Schroederichthys bivius		< 17	November
		26	November	21.95
		29	November	44.39		5.44	17.24
		30	November	47.14		7.76
		31/32	November	45.55		8.42	19.07
		32	November	64.87		10.25	18.09
		32	November	65.06		11.44	21.57
		32	November	74.75		11.72	16.37
		33	November	83.77		12.14	13.53

Oviparous chondrichthyans within Sub-Antarctic Marine Protected Areas “Namuncurá I” and “Namuncurá II” at Burdwood Bank, Argentina (Southwest Atlantic Ocean) were analyzed in this study, highlighting the importance that these areas have on the life cycle of chondrichthyan individuals. Nine species were found at the BB plateau and slope: Amblyraja doellojuradoi, Bathyraja albomaculata, B. macloviana, B. cousseauae, B. brachyurops, B. magellanica, B. multispinis, B. scaphiops, and Psammobatis rudis. The occurrence of P. rudis and B. cousseauae was reported for the first time in the BB. Other three skate species have been previously recorded in the area: Amblyraja georgiana, Bathyraja griseocauda, and Bathyraja meridionalis (Gosztonyi, 1981; Sabadin et al. 2020), adding up to 12 species at BB. Six of these 12 species are considered by the IUCN Red List as “Least Concern”, one as “Data Deficient”, three as “Near Threatened”, one as “Vulnerable”, and one as “Endangered”. Furthermore, the first records of oviparous chondrichthyans at Namuncurá II are presented since its creation in 2018: specimens of five species (B. albomaculata, B. multispinis, B. brachyurops, A. doellojuradoi, and P. rudis) and egg capsules of three (B. scaphiops, B. macloviana, and B. brachyurops) were recovered. Nonetheless, the presence of specimens of A. georgiana, B. griseocauda, and B. meridionalis have been reported in the area that currently corresponds to Namuncurá II in previous works (Gosztonyi 1981; Sabadin et al. 2020), raising the number of species up to 10.

Most of the hauls conducted in the BB area were monospecific for egg capsules, although richness of two and three were also found. These richness values are relatively lower than those reported by Vazquez et al. (2016) in the northern part of the Argentine Continental Shelf (nACS), who found richness up to five species per haul. Additionally, the highest general density was found at the NW Slope, and the highest densities for four species were found in the BB area (A. doellojuradoi, B. brachyurops, B. macloviana, and B. scaphiops).

Our results show the importance of the NW Slope as an egg-laying ground for A. doellojuradoi. Indeed, all the egg capsules (and a neonate) of this species were captured at the NW Slope, showing similar densities to those reported by Vazquez et al. (2016) at the nACS. Delpiani (2016) determined that A. doellojuradoi releases egg capsules year-round with a peak in autumn in the SWA between 36° and 50°S. This oviposition pattern is typical of deep-water species such as Amblyraja doellojuradoi (Hamlet and Koob 1999; Mabragaña and Cousseau, 2004; García et al. 2008; Delpiani 2016) because of the relatively stable condition of the environment (Hamlett and Koob 1999; Ruocco et al. 2006). Due to the lack of embryos for this species it is not possible to determine possible egg laying seasons for A. doellojuradoi in the BB. However, this area has relatively stable conditions (Cousseau et al. 1979; Falabella et al. 2017), suggesting that the oviposition pattern at BB could be similar to that proposed by Delpiani (2016).

The highest densities of egg capsules of B. brachyurops were found at Namuncurá I, indicating that this area is an important egg-laying ground for the species. The densities values were similar to those estimated at the nACS (Vazquez et al. 2016). Both Arkhipkin et al. (2008) and Vazquez et al. (2016) showed that most egg capsules of B. brachyurops were not found beyond 200–250 m depth, agreeing with our observations in the BB.

Namuncurá I and Namuncurá II were widely used as egg-laying grounds for B. macloviana. The highest density of egg capsules was found at Namuncurá I, where egg capsules with embryos and a neonate were also observed; the next highest density was recovered at Namuncurá II. The densities reported here were similar to those reported at the nACS (Vazquez et al. 2016). Females bearing egg capsules have been reported near the 200 m isobath around waters of Tierra del Fuego (Mabragaña et al. 2011), and in the shelf break around Falkland/Malvinas Islands (Arkhipkin et al. 2012). This information showed that the egg-laying grounds for B. macloviana would not be restricted to any particular area in the Patagonian shelf. Arkhipkin et al. (2012) found a year-round oviposition pattern in waters around Falkland/Malvinas Islands with seasonal peaks in autumn and spring. We found egg capsules with embryos in initial and advanced stages in autumn and winter, respectively. Vazquez (2020) estimated a minimum incubation time for B. macloviana (at 17°-23° C) of 157 days. This data, considering that incubation period is slower at lower temperatures (Berestovskii, 1994; Hoff, 2008; Vazquez, 2020), allowed us to predict that egg capsules with embryos in advanced stages had to be released at least the previous summer the cruise was conducted. Therefore, the oviposition at BB would take place, at least, in late summer and autumn.

Egg capsules of B. scaphiops were described a few years ago (Mabragaña et al. 2017), which probably explains the absence of data on egg-laying ground for this species. Here, we reported for the first time, egg laying ground for B. scaphiops in the Southwest Atlantic. The highest density of egg capsules was found in the slope at Namuncurá II, which remarks the importance of this area in the oviposition of this species.

Specimens of B. albomaculata were recovered both at Namuncurá I and Namuncurá II MPAs. Neither females bearing egg capsules nor egg capsules from seafloor were found in the study. Both Ruocco et al. (2006) and Mabragaña et al. (2011) registered females with egg capsules in the Argentine Continental Shelf at latitudes below 50ºS. Nonetheless, Arkhipkin et al. (2012), reported females bearing capsules near Falkland/Malvinas Islands, thus the possibility of reproductive activity of B. albomaculata at BB is not discarded.

We report here the first record of B. cousseauae at BB, specifically at Namuncurá I. Although there are no previous records of B. cousseaue at BB, the estimated occurrence probability was high at the BB slope (Sabadin et al. 2020). Nonetheless, individuals of B. cousseauae were not caught at Namuncurá II, probably due to the small number of hauls performed in the area. Egg capsules of this species were not found at BB; whereas Arkhipkin et al. (2012) registered egg capsules on the bottom in waters around the Falkland/Malvinas Islands and denoted that the oviposition is year-round, with seasonal peaks in late summer-autumn, and spring. Considering this and the fact that hauls were carried out in such seasons, it is likely that B. cousseauae does not use Namuncurá I as an oviposition area. Most specimens of this species, including a female bearing egg capsules (caught in autumn) and two egg capsules, were found at the CA, near Isla de los Estados, suggesting that these waters could be egg-laying grounds and that oviposition would happen at least in autumn.

Only one egg capsule of B. magellanica was found at Namuncurá I; whereas the majority of the egg capsules was recovered from the CA, including three egg capsules with embryos in advanced stages. Females bearing egg capsules were previously reported in late summer (February-March), both between 48°50´S and 50°30´S (Scenna and Díaz de Astarloa, 2014), and in Falkland/Malvinas Islands waters in the same months (Arkhipkin et al. 2012). Considering this pattern and knowing that the egg capsules with advanced and pre-hatching embryos found in this work were collected in spring (November), we suggest an incubation period of at least nine months for B. magellanica.

Two specimens of B. multispinis were collected at Namuncurá II: one neonate and one juvenile; whereas egg capsules were not observed. Further studies are required to determine whether Namuncurá II is used as an egg-laying ground or as a juvenile nursery ground. Females bearing eggs or egg capsules with embryos were not found around Falkland/Malvinas Islands (Arkhipkin et al. 2012). Previously, this species was registered at the BB surrounding slope, but not specifically at Namuncurá II (Sabadin et al. 2020).

An individual of the Bathyraja genus was captured at Namuncurá I (at 140 m depth), and the identification to species level was not possible. The specimen presented similar features with B. albomaculata but the dorsal face was covered with dermal denticles and the coloration was slightly different (Cousseau et al. 2007). Future genetic studies are required to confirm the identification of this specimen at species level.

Psammobatis rudis was registered for the first time at BB: both, specimens and egg capsules were captured. One individual was found at Namuncurá II (422 m) and another one at Namuncurá I (128 m). Sabadin et al. (2020) reported a low probability of occurrence in the area, but there were no reliable records so far. The highest density of egg capsules was found at the CA, near Isla de los Estados, where an egg capsule with an embryo was also collected. A similar value of density was observed at Namuncurá I. Therefore, both Isla de los Estados and Namuncurá I are egg-laying grounds for P. rudis.

Egg capsules of P. normani were only collected at the CA. Therefore, this area could be an egg-laying ground for this species, although the densities found were lower than those reported for the nACS and San Jorge Gulf (Vazquez et al. 2016; Ruibal Nuñez 2020). Mabragaña and Cousseau (2004) reported, for latitudes between 49° and 55°S, a pattern of oviposition in late summer. Females bearing egg capsules were found along the Argentinean Sea, including the San Jorge Gulf (Mabragaña et al. 2011; Ruibal Nuñez 2020). Neither specimens nor egg capsules of P. normani were found at BB. This result and the low probability of occurrence predicted by Sabadin et al. (2020), strongly indicates that this species does not inhabit at BB. In the same way, nor specimens/egg capsules of Z. brevicaudata were collected at BB. Sabadin et al. (2020) estimated a low occurrence probability in the area, therefore, it is likely that this species does not inhabit at BB.

Both specimens and egg capsules of S. bivius were only found at the CA. This result is consistent with previous records for this species (Gosztonyi 1981; Menni and Stehmann, 2000; Sabadin et al. 2020), and with the null probability of occurrence estimated for the BB (Sabadin et al. 2020). The highest egg capsules densities, the major number of specimens, and all the egg capsules with embryos were captured north of Tierra del Fuego in November. These features strongly suggest that Tierra del Fuego shelf is an important egg-laying ground for S. bivius, which could be associated with the high levels of primary productivity found at the area (Campagna et al. 2006). The egg capsules densities estimated were similar to those found at the nACS, and San Jorge Gulf (Vazquez et al. 2016; Ruibal Nuñez 2020). Additionally, a female-bearing eggs was captured in spring in the Beagle Channel, at 233 m depth. All the egg capsules with embryos in different stages, from initial to advanced, were captured in spring, suggesting a year-round oviposition pattern. Vazquez (2020) estimated 249–297 days the minimum incubation period for S. bivius at 7°-18° C. Therefore, the egg capsules with embryos in advanced stages may have been released in summer.

Egg-laying grounds for 5 oviparous chondrichthyans species within the BB area are reported here for the first time. The BB harbors at least 12 species of oviparous chondrichthyans, which represents almost the 70% of the diversity present in the Atlantic Sector of the Magellanic Province and Patagonian Slope Province (Cousseau et al. 2020; Sabadin et al. 2020). The importance of the NW Slope is also highlighted as the habitat and oviposition area for A. doellojuradoi. The NW Slope is not currently considered as a Marine Protected Area and it is not under any regulation. The information presented here should be taken into account and incorporated into the Management Plan of the MPA Namuncurá-Burdwood Bank. The monitoring of the NW Slope is required not only for its importance in the context of this work but also because of the high biodiversity and fragile ecosystems that harbors (Schejter and Bremec 2019). Finally, our results enhance the importance of Namuncurá II MPA as a habitat for 10 skate species and as oviposition area for at least two. Given their life history traits, overfishing is the key threat of chondrichthyan species especially on marine habitats (Dulvy et al. 2021). In this sense, effective MPAs emerge as one of the conservation actions that can provide species with refuge from fishing, at least from a fraction of their range (Dulvy et al. 2021). In Argentinean waters, known egg-laying and nursery areas within MPAs are under legislation that allows for fishing activities. In this regard, this study becomes relevant because it shows that the MPAs located at the BB allow protection of egg-laying grounds, critical areas for chondrichthyans´ survival according to The Important Shark and Ray Area (ISRA) approach, that provides a framework to identify areas of interest for the conservation of chondrichthyans based on different criteria, such as the presence of reproductive areas (sub-criteria C1) (Hyde et al. 2022). These results show the importance of the MPAs located at BB for the conservation of several species of oviparous chondrichthyans in southern waters of the South West Atlantic.

Acknowledgements

We would like to thank to the crew of the R/V “Puerto Deseado” (CONICET) and the R/V “Víctor Angelescu” for the assistance in the collection of samples. Also, to all the scientific staff for helping during sampling, as well as to Drs. Roccatagliata, Schejter, Riccialdelli, Diez and Alvarez Colombo for their commitment to coordinating the work on board. We are very grateful with Drs. Matias Delpiani and Gabriela Delpiani for their participation in the collection of the samples on board the research cruises. We want to thank the Consejo Interuniversitario Nacional as this study was carried out as part of an EVC grant. This work was part of F.M undergraduate thesis under supervision of E.M and D.M.V.

Author contributions

J.M.D.A. and E.M proposed and obtained funding for the project. E.M, D.M.V, and F.M. designed the study. E.M and D.M.V. collected the samples. F.M., D.M.V. and V.G. identified and measured the samples. F.M. carried out the analysis. F.M wrote the first version of the manuscript. All authors read and contributed critically to the drafts and gave final approval for publication.

Funding

This research was partly supported by funding from Agencia Nacional de Promoción Científica (Grant No. PICT 2018-2974, and PICT 2018-0790), Universidad Nacional de Mar del Plata (Grant No. EXA 970/20, and EXA 1069/22), and Consejo Nacional de Investigaciones Científicas y Técnicas CONICET (Grant No. PIP 11220200101475CO).

Data availability

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

Allega L, Braverman M, Cabreira AG, Campodónico S, Carozza CR, Cepeda GD, Colonello JH, Derisio C, Di Mauro R, Firpo CA, Gaitán EN, Hozbor MC, Irusta CG, Ivanovic M, Lagos N, Lutz VA, Marí NR, Militelli MI, Moriondo Danovaro PI, Navarro G, Orlando P, Pájaro M, Prandoni N, Prosdocimi L, Reta R, Rico R, Riestra CM, Ruarte C, Schejter L, Schiariti A, Segura V, Souto VS, Temperoni B, Verón E (2020) Estado del conocimiento biológico pesquero de los principales recursos vivos y su ambiente, con relación a la exploración hidrocarburífera en la Zona Económica Exclusiva Argentina y adyacencias. Instituto Nacional de Investigación y Desarrollo Pesquero INIDEP, Mar del Plata, 119 pp. http://hdl.handle.net/1834/17370.
Alverson DL, Pereyra WT (1969) Demersal fish explorations in the northeastern Pacific Ocean – an evaluation of exploratory fishing methods and analytical approaches to stock size and yield forecasts. J Fish Res Board Can 26:1985–2001. doi:10.1139/f69-188
Arkhipkin AI, Baumgartner N, Brickle P, Laptikhovsky VV, Pompert JHW, Shcherbich ZN (2008) Biology of the skates Bathyraja brachyurops and B. griseocauda in waters around the Falkland Islands, Southwest Atlantic. Ices J Mar Sci 65(4):560–570. https://doi.org/10.1093/icesjms/fsn015
Arkhipkin A, Brickle P, Laptikhovsky V, Pompert J, Winter A (2012) Skate assemblage on the eastern Patagonian Shelf and Slope: Structure, diversity and abundance. J Fish Biol 80(5):1704–1726. https://doi.org/10.1111/j.1095-8649.2012.03260.x
Ballard WW, Mellinger J, Lechenault H (1993) A Series of Normal Stages for Development of Scyliorhinus canicula, the Lesser Spotted Dogfish (Chondrichthyes: Scyliorhinidae). J Exp Zool 267:318-336. https://doi.org/10.1002/jez.1402670309
Becerril-García EE, Arauz R, Arellano-Martínez M, et al (2022) Research priorities for the conservation of chondrichthyans in Latin America. Biol Conserv 269:109535. https://doi.org/10.1016/j.biocon.2022.109535
Berestovskii EG (1994) Reproductive biology of skates of the family Rajidae in the Seas of the Far North. Journal of Ichthyology 34:26-37. https://doi.org/10.1007/s10152-011-0252-5.
Bremec CS, Schejter L, Gaitán E, Giberto D (2017) Banco Burdwood, Islas Georgias del Sur y Antártida. In: Bremec CS, Giberto DA (eds) Comunidades bentónicas en regiones de interés pesquero de la Argentina. Instituto Nacional de Investigación y Desarrollo Pesquero INIDEP, Mar del Plata, pp 77-92.
Brant FC (2006) Morfologia e Biometria do desenvolvimento embrionário da raia Sympterygia acuta Garman, 1877 (Elasmobranchii, Rajidae). Master´s dissertation, Federal University of Rio Grande, Brasil, 86 pp. http://repositorio.furg.br/handle/1/4194
Campagna C, Verona C, Falabella V (2006) Situación ambiental en la ecorregión del Mar Argentino. In: Brown A, Martínez Ortiz U, Acerbi M, Corcuera J (eds) La situación ambiental Argentina 2005. Fundación Vida Silvestre Argentina, Buenos Aires, pp 323- 336.
Collins AB, Heupel MR, Motta PJ (2007) Residence and movement patterns of cownose rays Rhinoptera bonasus within a south-west Florida estuary. J Fish Biol 71:1159-1178. https://doi.org/10.1111/j.1095-8649.2007.01590.x
Collins AB, Heupel MR, Simpfendorfer CA (2008) Spatial distribution and long-term movement patterns of cownose rays Rhinoptera bonasus within an estuarine river. Estuar Coast 31:1174-1183. https://doi.org/10.1007/s12237-008-9100-5
Costa TLA, Thayer JA, Mendes LF (2015) Population characteristics, habitat and diet of a recently discovered stingray Dasyatis marianae: implications for conservation. J Fish Biol 86:527−543. https://doi.org/10.1111/jfb.12572
Cousseau MB, Gru DL, Hansen JE (1979) Campañas realizadas por el buque de investigación" Shinkai Maru" en el Mar Argentino, desde abril de 1978 hasta abril de 1979. Organización y reseña de datos obtenidos. Contribuciones Instituto Nacional de Investigaciones y Desarrollo Pesquero INIDEP, Mar del Plata 373:1–625.
Cousseau MB, Figueroa DE, Díaz de Astarloa JM, Mabragaña E, Lucifora LO (2007) Rayas, chuchos y otros batoideos del Atlántico Sudoccidental (34°S-55°S). Publicaciones especiales INIDEP, Mar del Plata, 102 pp.
Cousseau MB, Pequeño G, Mabragaña E, Lucifora LO, Martínez P, Giussi A (2020) The Magellanic Province and its fish fauna (South America): several provinces or one? J Biogeogr 47:220-215. https://doi.org/10.1111/jbi.13735
Covatti Ale M, Fischer L, Deli Antoni M, Diaz de Astarloa JM, Delpiani G (2022) Trophic ecology of the yellowfin notothen, Patagonotothen guntheri (Norman, 1937) at the Marine Protected Area Namuncurá-Burdwood Bank, Argentina. Polar Biol 45:549–558. https://doi.org/10.1007/s00300-022-03011-w
Dean MN, Bizzarro JJ, Clark B, Underwood CJ, Johanson Z (2017) Large batoid fishes frequently consume stingrays despite skeletal damage. R Soc Open Svi 4:170674. https://doi.org/10.1098/rsos.170674
Delpiani G (2016) Reproductive biology of the southern thorny skate Amblyraja doellojuradoi (Chondrichthyes, Rajidae). J Fish Biol 88(4):1413–1429. https://doi.org/10.1111/jfb.12917
Delpiani SM, Bruno DO, Vazquez DM, Llompart F, Delpiani GE, Fernández DA, Rosso JJ, Mabragaña E, Díaz de Astarloa JM (2020) Structure and distribution of fish assemblages at Burdwood Bank, the first Sub-Antarctic Marine Protected Area “Namuncurá” in Argentina (Southwestern Atlantic Ocean). Polar Biol 43(11):1783–1793. https://doi.org/10.1007/s00300-020-02744-w
Dulvy NK, Pacoureau N, Rigby CL, Pollom RA, et al (2021). Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Curr Biol 31(21):4773-4787. https://doi.org/10.1016/j.cub.2021.08.062
Dunne JA, Williams RJ, Martinez ND (2004) Network structure and robustness of marine food webs. Mar Ecol Prog Ser 273:291-302. https:// doi:10.3354/meps273291
Ellis JR, Cruz-Martinez A, Rackham BD, Rogers SI (2005) The distribution of chondrichthyan fishes around the British Isles and implications for conservation. J Northw Atl Fish Sci 35(5):195−213. http://doi: 10.2960/J.v35.m485
Falabella V, Campagna C, Caille G, Krapovickas S, Moreno D, Michelson A, Piola A, Schejter L, Zelaya D (2017) Banco Burdwood: Contribuciones para el establecimiento de una línea de base y plan de manejo de la futura Área Marina Protegida. Jefatura de Gabinete de Ministros. Buenos Aires, Argentina, 76 pp.
Figueroa DE (2011) Clave ilustrada de Agnatos y Peces Cartilaginosos de Argentina y Uruguay. In: Wölher OC, Cedrola P, Cousseau MB (eds) Contribuciones sobre biología, pesca y comercialización de tiburones en la Argentina. Aportes para la elaboración del Plan de Acción Nacional. Buenos Aires, Consejo Federal Pesquero, Buenos Aires, pp 25-74.
Fischer L, Covatti Ale M, Deli Antoni M, Díaz de Astarloa JM, Delpiani G (2022) Feeding ecology of the longtail southern cod, Patagonotothen ramsayi (Regan, 1913) (Notothenioidei) in the Marine Protected Area Namuncurá-Burdwood Bank, Argentina. Polar Biol, 1-12. https://doi.org/10.1007/s00300-022-03082-9
Gabbanelli V, Díaz de Astarloa JM, González-Castro M, Vazquez DM, Mabragaña E (2018) Almost a century of oblivion: Integrative taxonomy allows the resurrection of the longnose skate Zearaja brevicaudata (Marini, 1933) (Rajiformes; Rajidae). C R Biol 341(9–10):454–470. https://doi.org/10.1016/j.crvi.2018.10.002
García VB, Lucifora LO, Myers RA (2008) The importance of habitat and life history to extinction risk in sharks, skates, rays and chimaeras. P Roy Soc B-Biol Sci 275(1630):83–89. https://doi.org/10.1098/rspb.2007.1295
Gosztonyi A (1981) Resultados ictiológicos de la primera campaña de investigaciones pesqueras del buque “Shinkai Maru” en aguas argentinas. In: Angelescu V (ed) Campañas de investigación pesquera realizadas en el Mar Argentino por los B/I “Shinkai Maru” y “Walther Herwig” y el B/P “Marburg”, años 1978 y 1979. Resultados de la parte argentina. Contribuciones Instituto Nacional de Investigaciones y Desarrollo Pesquero INIDEP, Mar del Plata 383, 254-266.
Hamlett WC, Koob TJ (1999) Female reproductive system. In: WC Hamlett (ed) Sharks, skates and rays. The biology of elasmobranch fishes. Baltimore: Johns Hopkins University Press, pp 398-443.
Heithaus MR, Frid A, Vaudo JJ, Worm B, Wirsing AJ (2010) Unraveling the Ecological Importance of Elasmobranchs. In Carrier JC, Musick JA, Heithaus MR (Eds) Sharks and Their Relatives II: Biodiversity, Adaptive Physiology, and Conservation. CRC Press, Boca Raton: 611–638. https://doi.org/10.1201/9781420080483-c16
Henry LA, Navas JM, Hennige SJ, Wicks LC, Vad J, Roberts JM (2013) Cold-water coral reef habitats benefit recreationally valuable sharks. Biol Conserv 161:67–70. https://doi.org/10.1016/j.biocon.2013.03.002
Hoff GR (2006) Biodiversity as an index of regime shift in the eastern Bering Sea. Fish Bull. 104:226−237. http://hdl.handle.net/1834/25605
Hoff GR (2007) Reproductive biology of the Alaska skate Bathyraja parmifera, with regard to nursery sites, embryo development and predation. PhD dissertation, University of Washington, Seattle, WA
Hoff, GR (2008). A nursery site of the Alaska skate (Bathyraja parmifera) in the eastern Bering Sea. Fish Bull 106: 233–244. http://hdl.handle.net/1834/25478
Hunt JC, Lindsay DJ, Shahalemi RR (2011) A nursery site of the golden skate (Rajiformes: Rajidae: Bathyraja smirnovi) on the Shiribeshi Seamount, Sea of Japan. Mar Biodivers Rec 4, 1-7. https://doi.org/10.1017/S1755267211000728
Hyde CA, Notarbartolo di Sciara G, Sorrentino L, Boyd C, Finucci B, Fowler SL, Kyne PM, Leurs G, Simpfendorfer CA, Tetley MJ, Womersley F, Jabado RW (2022) Putting sharks on the map: A global standard for improving shark area-based conservation. Front Mar Sci, 1660. https://doi.org/10.3389/fmars.2022.968853
Jañez JA, Sueiro MC (2007) Size at hatching and incubation period of Sympterygia bonapartii (Müller & Henle, 1841) (Chondrichthyes, Rajidae) bred in captivity at the Temaiken Aquarium. J Fish Biol 70: 648-650. https://doi.org/10.1111/j.1095-8649.2007.01332.x
Love MS, Schroeder DM, Snook L, York A, Cochrane G (2008) All their eggs in one basket: a rocky reef nursery for the longnose skate (Raja rhina Jordan and Gilbert, 1880) in the southern California Bight. Fish Bull 106:471-475. http://hdl.handle.net/1834/25476
Lucifora LO, García VB (2004) Gastropod predation on egg cases of skates (Chondrichthyes, Rajidae) in the southwestern Atlantic: quantification and life history implications. Mar Biol 145(5):917-922. ttps://doi.org/10.1007/s00227-004-1377-8
Mabragaña E, Cousseau MB (2004) Reproductive biology of two sympatric skates in the south-west Atlantic: Psammobatis rudis and Psammobatis normani. J Fish Biol 65:559-573. https://doi.org/10.1111/j.0022-1112.2004.00473.x
Mabragaña E, Figueroa DE, Scenna LB, Díaz de Astarloa JM, Colonello JH, Delpiani G (2011) Chondrichthyan egg cases from the south-west Atlantic Ocean. J Fish Biol 79:1261–1290. https://doi.org/10.1111/j.1095-8649.2011.03111.x
Mabragaña E, Lucifora LO, Corbo ML, Díaz de Astarloa JM (2015) Seasonal Reproductive Biology of the Bignose Fanskate Sympterygia acuta (Chondrichthyes, Rajidae). Estuar Coast 38: 1466‐1476. https://doi.org/10.1007/s12237-014-9888-0
Mabragaña E, Vazquez DM, Gabbanelli V, Sabadin D, Barbini S, Lucifora L (2017) Egg cases of the graytail skate Bathyraja griseocauda and the cuphead skate B. scaphiops from the Southwest Atlantic. J Fish Biol 91:968–974. https://doi.org/10.1111/jfb.13380
Martins AP, Heupel MR, Chin A, Simpfendorfer CA (2018) Batoid nurseries: definition, use and importance. Mar Ecol Prog Ser 595: 253-267. https://doi.org/10.3354/meps12545
Massa A, Lucifora LO, Hozbor NM (2004) Condrictios de las regiones costeras bonaerense y uruguaya. In: Boschi EE (ed) El Mar Argentino y sus recursos pesqueros Vol 4. Los peces marinos de interés pesquero. Caracterización biológica y evaluación del estado de explotación. Publishers INIDEP, Mar del Plata, 85-99 pp.
Menni RC, Stehmann M (2000) Distribution, environment and biology of batoid fishes off Argentina, Uruguay and Brazil. A review. Revista del Museo Argentino de Ciencias Naturales, 1(2):69–109.
Musick JA, Ellis JK (2005) Reproductive evolution of chondrichthyans. In: Hamlett WC (ed) Reproductive biology and phylogeny of chondrichthyes: sharks, rays and chimaeras, Vol. 3. Endfield, USA: Science Publishers. 45‐79 pp
Navia AF, Mejia-Falla PA, Lopez-Garcia J, Giraldo A, Cruz-Escalona VH (2017) How many trophic roles can elasmobranchs play in a marine tropical network? Mar Freshw Res 68:1342-1353. https://doi.org/10.1071/MF16161
Okonski SL, Martini LW (1987) Artes y Métodos de pesca. Materiales didácticos para la capacitación técnica (Vol. 339). Buenos Aires: Hemisferio Sur.
Roberts CM, O´Leary BC, McCauley DJ, et al (2017) Marine reserves can mitigate and promote adaptation to climate change. Proc Natl Acad Sci 114:6167–6175. https://doi.org/10.1073/pnas.1701262114
Roff G, Doropoulos C, Rogers A, Bozec YM, Krueck NC, Aurellado E, Priest M, Birrell C, Mumby PJ (2016) The Ecological Role of Sharks on Coral Reefs. Trends Ecol Evol, 31(5), 395–407. https://doi.org/10.1016/j.tree.2016.02.014
Ruibal Núñez J (2020) Impacto ecológico de la actividad pesquera en las poblaciones de condrictios en el litoral de la Provincia de Chubut y Golfo San Jorge. PhD dissertation, National University of Mar del Plata, Argentina, 269 pp.
Ruocco NL, Lucifora LO, Díaz De Astarloa JM, Wöhler O (2006) Reproductive biology and abundance of the white-dotted skate, Bathyraja albomaculata, in the Southwest Atlantic. Ices J Mar Sci 63(1):105–116. https://doi.org/10.1016/j.icesjms.2005.08.007
Sabadin DE, Lucifora LO, Barbini SA, Figueroa DE, Kittlein M (2020) Towards regionalization of the chondrichthyan fauna of the Southwest Atlantic: a spatial framework for conservation planning. Ices J Mar Sci 77(5):1893–1905. https://doi.org/10.1093/icesjms/fsaa064
Sánchez RP (2010). Implementación del Plan de Acción Nacional para la Conservación y el Manejo de los Tiburones (PAN-Tiburones) en la República Argentina1. Frente Maritimo, 21, 163.
Scenna LB (2011) Biología y ecología reproductiva de las especies del género Bathyraja (Elasmobranchii, Rajidae) en la plataforma continental argentina. PhD dissertation, National University of Mar del Plata, Argentina, 183 pp.
Scenna LB, Díaz De Astarloa JM (2014) Reproductive biology of the Magellan skate, Bathyraja magellanica (Chondrichthyes, Rajidae), in the south-western Atlantic. Mar Freshw Res 65(9): 766–775. https://doi.org/10.1071/MF13144
Schejter L, Bremec CS (2019) Stony corals (Anthozoa: Scleractinia) of Burdwood Bank and neighbouring areas, SW Atlantic Ocean. Sci Mar 83(3):247-260.
Schejter L, Rimondino C, Chiesa I, Díaz de Astarloa JM, Doti B, Elías R, Escolar M, Genzano G, López-Gappa J, Tatián M, Zelaya DG, Cristobo J, Perez CD, Cordeiro RT, Bremec CS (2016) Namuncurá Marine Protected Area: an oceanic hot spot of benthic biodiversity at Burdwood Bank, Argentina. Polar Biol 39(12):2373–2386. https://doi.org/10.1007/s00300-016-1913-2
Schejter L, Martin J, Lovrich G (2017) Unveiling the submarine landscape of the Namuncurá Marine Protected Area, Burdwood Bank, SW Atlantic Ocean. Pan-Am J Aquat Sci, 12(3):248–253.
Schejter L, Genzano G, Gaitán E, Perez CD, Bremec CS (2020) Benthic communities in the Southwest Atlantic Ocean: Conservation value of animal forests at the Burdwood Bank slope. Aquat Conserv 30(3):42 6– 439. https://doi.org/10.1002/aqc.3265
Sheaves M (2009) Consequences of ecological connectivity: the coastal ecosystem mosaic. Mar Ecol Prog Ser 391:107-115. https://doi.org/10.3354/meps08121
Stevens JD, Bonfil R, Dulvy NK, Walker PA (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. Ices J Mar Sci 57:476-494. https://doi.org/10.1006/jmsc.2000.0724
Treude T, Kiel S, Linke P, Peckman J, Goedert JL (2011) Elasmobranch egg capsules associated with modern and ancient cold seeps: a nursery for marine deep-water predators. Mar Ecol Prog Ser 437:175-181. https://doi.org/10.3354/meps09305
Vaudo JJ, Heithaus MR (2011) Dietary niche overlap in a nearshore elasmobranch mesopredator community. Mar Ecol Prog Ser 425:247-260. https://doi.org/10.3354/meps08988
Vazquez DM (2020) Desarrollo embrionario en condrictios ovíparos del Mar Argentino: importancia para su conservación. PhD dissertation, National University of Mar del Plata, Argentina, 196 pp.
Vazquez DM, Mabragaña E, Gabbanelli V, Díaz de Astarloa JM (2016) Exploring nursery sites for oviparous chondrichthyans in the southwest Atlantic (36º-41ºS). Mar Biol Res 12:715-725. https://doi.org/10.1080/17451000.2016.1203948
Vazquez DM, Belleggia M, Schejter L, Mabragaña E (2018) Avoiding being dragged away: finding of egg cases of Schroederichthys bivius (Chondrichthyes: Scyliorhinidae) associated with benthic invertebrates. J Fish Biol 92: 248–253. https://doi.org/10.1111/jfb.13490
Weigmann S, Stehmann MFW, Bürkel DL (in press) Order Rajiformes -Skates. In: Gon O, Gon J (eds) Fishes of the Southern Ocean, 2nd edition. NISC (Pty) Ltd, Grahamstown
Zunino G, Ichazo MM (1979) Los peces demersales del Banco Burdwood: distribución, abundancia de las especies y frecuencia de tallas (según datos de los B/I Walther Herwig y Shinkai Maru, campañas 1978–1979). Final report, Oceanografía Biológica, Universidad de Buenos Aires, 66 pp

No competing interests reported.

OnlineResources.pdf

Download PDF

Journal Publication

published 08 Apr, 2023

Read the published version in Polar Biology →

Editorial decision: Major revision
25 Feb, 2023
Reviews received at journal
31 Jan, 2023
Reviewers agreed at journal
11 Jan, 2023
Reviewers invited by journal
15 Dec, 2022
Editor assigned by journal
13 Dec, 2022
Submission checks completed at journal
08 Dec, 2022
First submitted to journal
07 Nov, 2022

You are reading this latest preprint version

Chondrichthyan fauna from the Marine Protected Area Namuncurá at Burdwood Bank: exploring egg nursery grounds

Status:

Journal Publication

Version 1

Abstract

Figures

Introduction

Materials And Methods

Sample collection

Sample identification

Occurrence, richness, and abundance patterns

Embryonic development

Results

Specimen occurrence patterns

Egg capsule occurrence patterns

Egg capsule richness and abundance patterns

Embryonic development

Discussion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Journal Publication

Version 1