Habitat use, seasonality and demography of the broadnose sevengill shark Notorynchus cepedianus in central Patagonia: Another piece of the puzzle
Abstract
enThe habitat use, seasonality and demography of the broadnose sevengill shark Notorynchus cepedianus were investigated in central Patagonia, where a data gap exists for the species. Catch and effort and video-derived indices indicated high relative abundance of sharks during warm months. Video stations revealed differences in the spatial use by sharks, being more frequently observed in the inner section of the bay. Complementary tagging efforts evidenced both a seasonal residence pattern and site fidelity between consecutive warm seasons. Juveniles outnumbered adults, which suggests that they may use the study area as a secondary nursing ground. Evidence from spontaneous regurgitation further suggests that prey abundance may be driving the seasonal occurrence of sharks in the region. This study allows for a more comprehensive understanding of the population structure and dynamics of sevengill sharks in the Southwest Atlantic.
Abstract
esEl uso de hábitat, estacionalidad y demografía del tiburón gatopardo (Notorynchus cepedianus) fue investigado en Patagonia Central, donde existe un vacío de datos para la especie. Seis campañas de investigación fueron llevadas a cabo bimensualmente entre 2018 y 2019 en Caleta Malaspina (45º10'S–66º35'O, Chubut), durante las cuales se realizaron sesiones de pesca y se logró capturar y marcar un total de 88 ejemplares (65 hembras, 23 machos). A partir de estas capturas se obtuvieron datos biológicos (i.e. largo total, sexo, marcas de cópula, recapturas) y se estudió el patrón estacional de abundancia de la especie. Estos datos se complementaron con registros de estaciones subacuáticas de video fijas con cebo (ESVFC) en tres secciones de la caleta (interna, media y externa) para determinar diferencias espaciales en el uso de la misma. Los cuatro índices de abundancia relativa construidos, la Captura por Unidad de Esfuerzo (CPUE a partir de las sesiones de pesca) y tres índices de abudancia a partir del análisis de las ESVFC (MaxN, MaxNIND y Nocc), indicaron altas abundancias durante los meses cálidos y bajas o nulas durante la temporada fría. Las ESVFC revelaron que la sección interna de la caleta es más frecuentemente utilizada por los tiburones. Tres recapturas sugirieron un patrón de residencia estacional y fidelidad al sitio en temporadas cálidas consecutivas. Los individuos juveniles superaron en gran medida a los adultos, lo cual sugiere que podrían utilizar la caleta como un área de cría secundaria. Adicionalmente, a partir del análisis de contenidos estomacales obtenidos en regurgitaciones espontáneas se infiere que la abundancia de lobos marinos (Mirounga leonina), la principal presa encontrada, podría explicar la ocurrencia estacional del gatorpardo en la región. Este estudio permite un entendimiento más acabado de la estructura y dinámica poblacional del tiburón gatopardo en el Atlántico Sudoccidental.
Introduction
Animal movement and its relation with the environment represent crucial ecological knowledge for successful management and conservation strategies at multiple spatial scales (Humphries et al. 2010; Block et al. 2011; Avgar et al. 2013). In the case of large sharks, movement information is usually scarce and scattered due to our limitations to survey the marine environment, also exacerbated by their widespread long-scale migrations (Papastamatiou et al. 2013). Compared to other marine animal groups, in general large sharks occur in low densities, have elusive behaviour and distribute over vast areas that are usually inaccessible by standard research methods (Heithaus et al. 2008; Heupel et al. 2015). Furthermore, their migratory patterns are known to be complex as a result of sexual- and/or life-history stage-specific inequities (Chapman et al. 2012; Papastamatiou et al. 2013).
The broadnose sevengill shark Notorynchus cepedianus (Péron 1807) is a highly migratory species occurring in most temperate coastal and continental shelf marine environments (Compagno 2009; Last & Stevens 2009). This shark is an upper predator that exerts top-down effects by influencing the population of other predators (e.g. marine mammals), highlighting their important role in marine ecosystems (Barnett et al. 2012). Despite worldwide efforts have been made to increase knowledge on the species, available information remains limited to assess its conservation status (Compagno 2009). Furthermore, the species is highly vulnerable to overfishing in many parts of the world as a consequence of exposure to coastal fisheries. In the Patagonian region of the Southwest Atlantic, for example, N. cepedianus is widely targeted by anglers (e.g. Cedrola et al. 2009) and incidentally caught in the prawn (Pleoticus muelleri) and argentine hake (Merluccius hubbsi) fisheries, with frequencies of occurrence decreasing from a maximum of 2.7% of hauls in the 1990s (Van Der Molen et al. 1998) to 0.4% in the period 2005–2014 (Ruibal Núñez et al. 2018). Such findings are in line with recent studies in the region that by using different data sources and methods have demonstrated a serious decline of N. cepedianus abundance over the last four decades (Barbini et al. 2015; Irigoyen & Trobbiani 2016). Biological life-history traits including slow growth and long-term maturation (Compagno 2009) raise further concern about its conservation status.
In the Southwest Atlantic, N. cepedianus is mostly distributed within the Argentinian coast (34–50°S), being found occasionally as far north as Cananéia, Brazil (25°S; Sadowsky 1970), and as far south as Dungeness cape, Chile (52°S; Guzmán & Campodónico 1976). To date, few studies describe N. cepedianus occurrence in bays and estuaries along the Argentinian coast, highlighting latitudinal differences in abundance and size throughout seasons. Young individuals (<100 cm LT) mainly inhabit northern areas from the southern boundary of the Río de la Plata (36°30′S; Milessi et al. 2019) to Anegada Bay (40°30′S; Lucifora et al. 2005) with higher occurrence during summer. Juveniles (males <170 cm LT, females <190 cm LT) present a wider distribution, being recorded in several places including southern Río de la Plata (De Wysiecki et al. 2018), Anegada Bay (Lucifora et al. 2005), Valdés Peninsula (42°30′S; Irigoyen et al. 2018), Ria Deseado (47°30′S; Cedrola et al. 2009) and San Julián Bay (49°30′S, Cedrola et al. 2009). Differences in seasonal occurrence have been described for juveniles, ranging from early spring in northern areas to late summer in southern areas, and recently, a nearly permanent occurrence has been described in northern Patagonia between the extremes of its distribution (Irigoyen et al. 2018). Adults showed similar seasonality compared to juveniles in most coastal habitats, except in the southernmost areas where their abundance is low or null (Cedrola et al. 2009). Therefore, an important shift in population structure of sevengill sharks is expected to occur along Patagonian waters, from a co-occurring juvenile–adult structure to only juveniles.
The aim of this study was to determine the habitat use, seasonal pattern of abundance and demographic structure of N. cepedianus in central Patagonia where a data gap exists. To achieve this, we use a combination of fishery-independent methods over an entire year. This study complements recent findings of the species in northern Patagonia (Irigoyen et al. 2018) and also contributes to an overall understanding of the species dynamics in the Southwest Atlantic.
Methods
Study site
Study site was Caleta Malaspina (central Patagonia, Fig. 1), a marine bay that falls geographically in the centre of the coast span where a data gap exists for N. cepedianus. The site was also chosen among neighbouring because there were reports of high abundance of these sharks from informal interviews with local anglers and divers (A. Irigoyen, unpubl. data, 2012). The area is located at the north extreme of San Jorge Gulf and within a coastal marine protected area (MPA) ‘The Interjurisdictional Marine Coastal Park Patagonia Austral (PIMCPA)’.
Caleta Malaspina is a 10-km-long bay with a narrow mouth, seven islands and many islets. The bay is comprised of three sections. The inner section of the bay is characterised by soft bottoms (mud and sand) and a central deep channel (between 8 and 19 m deep depending on tide) surrounded by shallow bays and large intertidal areas. This section possesses two penguin colonies located in two islands that are connected by land at low tides. The mouth section, which connects to the open sea, is characterised by rocky and gravel bottoms and relatively shallow depths (between 3 and 10 m depending on tide). Five islands are located in this portion of the bay, which are seasonally occupied by South American sea lions (Otaria flavescens) and seabirds (Yorio et al. 1998; Grandi et al. 2008). The outer (defined here as the area adjacent to the mouth) portion of the bay is characterised by irregular rocky bottoms with patchy kelp forests of Macrocystis pyrifera. Along the bay, tides produce strong currents of changing direction throughout its constant cycle. Currents are particularly strong in the mouth section of the bay due to its narrower and shallower nature (A. Irigoyen, pers. obs.). Water surface temperature fluctuates seasonally between a mean value of 10.5°C in September and 17.9°C in March (monthly SST for the year 2018, Aqua MODIS, data not published). The terrestrial environment is characterised by hard weather conditions, mainly for the presence of strong winds and extreme temperatures (A. Irigoyen, pers. obs.).
Two of the islands located in the mouth of the bay support breeding rockeries and haul-out sites for sea lions, which aggregate between December and March with breeding and mating purposes (Reyes & García-Borboroglu 2004). The rest of the year, individuals disaggregate but remain in the region. Furthermore, populated colonies of O. flavescens are located a few kilometres north and south of Caleta Malaspina (Grandi et al. 2008).
Field methods and sampling design
Three-day-long sampling trips were conducted bimonthly between January 2018 and January 2019. Site and tide variables were fixed to avoid effects on relative abundance estimates. Sampling was done only on days with low tide occurring at midday (between 11.00 and 14.00 hours). Two approaches were used to capture information on these sharks:
Rod and reel fishing
At least two fishing sessions per sampling trip were performed from the coast in order to calculate a catch-per-unit-effort (CPUE) index of relative abundance. The sampling site (‘Playa Nelson’, Fig. 1) was chosen for its accessibility by land with motor vehicles. Fishing sessions varied between 3 and 6 h long and were conducted between 16.00 and 23.00 hours using either four or five fishing rods depending on available personnel. Each rod and reel possessed one hook (Mustad 2330-DT, size 1) baited with Atlantic chub mackerel (Scomber colias). Fishing lines were cast between 5 and 20 m from shore. An additional two fishing sessions—not included in the sampling design or CPUE analysis – were opportunistically performed on 18 January 2018 and 21 January 2019 with the sole purpose of increasing the number of sharks tagged and sampled in this study. During handling [see Irigoyen et al. (2018) for procedure details], all individuals were sexed, measured (total length, LT to the nearest cm) and tagged with dart tags (FT-1-94; Floy Tag Inc.). In addition, female individuals were visually inspected in order to record the presence of fresh mating scars.
Baited remote underwater video stations
Baited remote underwater video stations (BRUVS) deployments were conducted to calculate fishing-independent indices of relative abundance in order to corroborate those estimated by the fishing method. To explore spatial differences in shark's abundance, we selected three BRUVS deployment sites along the bay: inner, mouth and outer sections (Fig. 1). Five BRUVS were deployed per section from a total of 15 units per sampling trip. BRUVS were positioned in the 3–12 m deep range between 1 h before and 1 h after high tide, to avoid the highest current areas and moments detected on the first field trip (January 2018). The first 60 min (approximately 30 min before and after high tide) of video imagery was analysed to ensure the most stable physical conditions at high tide on each session. We used Atlantic chub mackerel S. colias as bait for all deployments. More details on devices, deployment procedure and relative abundance indices (MaxN, MaxNIND and Nocc) can be found in Irigoyen et al. (2018). To evidence further possible differences between deployment sites, we constructed an additional index, the FO, as the time (expressed in minutes) of first occurrence of N. cepedianus in the video session deployed. For comparison among samples, when sharks were not recorded in a single deployment, FO was set at 60 min.
Analyses
Catch- and BRUVS-derived estimates were used to investigate N. cepedianus population structure and abundance fluctuation. The CPUE was defined as the number of N. cepedianus caught divided by the number of hooks and soak time for each rod and reel fishing session. Juveniles and adults were differentiated by taking into account the onset size at gonadal maturity estimated in Irigoyen et al. (2018) (females = 190 cm LT, and males = 170 cm LT). The sex ratio (female:male) for juvenile and adult stages was calculated for the population. Possible differences in the spatial use of the area were also explored for the study period by comparing BRUVS indices between the three sections (inner, mouth and outer; anova test). Additionally, since spontaneous regurgitation is common during handling of captured individuals, stomach contents were opportunistically collected. Regurgitated prey item was identified to the lowest possible taxonomic level. Finally, any recaptures of tagged individuals were recorded to contribute to the understanding of the movement of these sharks. All analyses were done in R software (R Core Team, 2018).
Results
Over the course of the study, a total of 88 sharks (65 females and 23 males, sex ratio 2.8:1) were sampled and safely released back into the water. Females ranged between 128 and 225 cm LT (mean LT = 181 cm), and males ranged between 121 and 178 cm LT (mean LT = 154 cm). The length–frequency distribution presented significant differences between sexes (W = 1226, P = 5.612e−06, Wilcoxon rank test) with females being larger than males (Fig. 2). No evident visual differences in size range were found between sharks caught through fishing or spotted on BRUVS. With the exception of seven school sharks (Galeorhinus galeus) caught on January 2019, no other fish species were captured. Water temperature taken in the field ranged between 9°C in June and September to 18°C in January.
Population structure and abundance
Notorynchus cepedianus BRUVS-derived and CPUE relative abundance indices showed fluctuations over the period of this study (Figs 3, 4). In general, all indices showed high relative abundances during warm months (late austral spring–summer), as opposed to the rest of the year when minimum values were recorded. During the autumn (June) survey, sharks were neither caught nor spotted on BRUVS. Catch-per-unit-effort index varied from 0.88 sharks per hook−1 h−1 to a null catch. Catches were dominated by females and juveniles (Fig. 4). Further, adults fell within the lower LT range of the species for the region [see Fig. 2 in Irigoyen et al. (2018)].
Baited remote underwater video stations-derived indices showed significant differences in relative abundance between the three sections of the bay: MaxN (anova, F = 11.7, P < 0.0001), MaxNIND (anova, F = 10.6, P < 0.0001) and Nocc (anova, F = 9.0, P = 0.0003). These indices indicated that the inner section of the inlet consistently had higher relative abundance compared to mouth or outer sections (Table 1). The FO index values were significantly different among the three sections considered (anova, F = 19.7, P < 0.0001), with shorter times of first occurrence recorded at the inner section of the bay (inner = 31.4 ± 11.8, mouth = 53.6 ± 9.4 and outer = 59.7 ± 0.7). It is important to mention that only two BRUVS deployments were successfully retrieved during the first summer sampling trip (January 2018), because most devices were severely drifted by currents and one device was lost (see Methods).
| Month-year | Bay section | Temperature (ºC) | Current (1–4) | Visibility (m) | BRUVS indices ± SD | N BRUVS (N positive) | |||
|---|---|---|---|---|---|---|---|---|---|
| FO (min) | MaxN | MaxNIND | Nocc | ||||||
| January-18 | Inner | 18.0 | 2.0 | 4.0 | 18.0 ± 2.8 | 1.5 ± 0.7 | 3.0 ± 0.0 | 41.0 ± 7.1 | 2 (2) |
| March-18 | Inner | 14.7 | 2.0 | 7.5 | 30.2 ± 11.2 | 1.5 ± 0.6 | 2.3 ± 0.5 | 36.3 ± 15.0 | 4 (4) |
| June-18 | Inner | 9.0 | 2.0 | 5.0 | 60.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 5 (0) |
| September-18 | Inner | 9.0 | 2.5 | 4.7 | 33.9 ± 14.7 | 0.7 ± 0.5 | 0.7 ± 0.5 | 3.7 ± 4.0 | 6 (3) |
| November-18 | Inner | 13.5 | 1.8 | 4.5 | 16.3 ± 2.2 | 2.3 ± 1.0 | 4.0 ± 2.4 | 69.0 ± 48.7 | 4 (4) |
| January-19 | Inner | 18.0 | 2.0 | 2.4 | 27.0 ± 9.6 | 1.2 ± 0.8 | 2.0 ± 1.4 | 38.6 ± 23.6 | 5 (4) |
| January-18 | Mouth | 18.0 | 2.0 | 6.5 | 60.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 2 (0) |
| March-18 | Mouth | 14.7 | 2.4 | 3.4 | 49.2 ± 19.7 | 0.6 ± 0.5 | 0.6 ± 0.5 | 0.0 ± 0.0 | 5 (2) |
| June-18 | Mouth | 9.0 | 3.0 | 7.0 | 60.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 4 (0) |
| September-18 | Mouth | 9.0 | 4.5 | 8.5 | 60.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 4 (0) |
| November-18 | Mouth | 13.5 | 1.6 | 4.8 | 48.6 ± 18.8 | 0.6 ± 0.9 | 1.2 ± 2.2 | 10.8 ± 23.6 | 5 (2) |
| January-19 | Mouth | 18.0 | 2.6 | 3.8 | 44.0 ± 11.0 | 0.4 ± 0.5 | 0.4 ± 0.5 | 4.0 ± 7.9 | 5 (1) |
| January-18 | Outer | 18.0 | 1.0 | 8.0 | 60.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 1 (0) |
| March-18 | Outer | 14.7 | 2.8 | 2.0 | 60.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 4 (0) |
| June-18 | Outer | 9.0 | 2.0 | 7.5 | 60.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 4 (0) |
| September-18 | Outer | 9.0 | 2.5 | 8.0 | 60.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 4 (0) |
| November-18 | Outer | 13.5 | 1.3 | 4.0 | 58.3 ± 26.5 | 0.5 ± 1.0 | 0.5 ± 1.0 | 6.3 ± 12.5 | 4 (1) |
| January-19 | Outer | 18.0 | 2.0 | 5.0 | 60.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 0.0 ± 0.0 | 4 (0) |
School sharks (G. galeus) were also observed on BRUVS at the outer section of the bay on March 2018 and at the inner section on January 2019. No other chondrichthyan species were recorded. Also, schools of silversides (Odontesthes smitti) were relatively abundant in all video sessions, whereas solitary individuals of morwong (Nemadactylus bergi), juveniles of rockfish (Sebastes oculatus) and Patagonian blenny (Eleginops maclovinus) were recorded only in few occasions.
Qualitative prey data and recaptures
A total of 11 individuals (12.5%) regurgitated stomach contents as a result of gastric eversion during handling on the shore. During summer surveys, six individuals regurgitated chunks of South American sea lion (O. flavescens), and in different times along the year, four individuals regurgitated whole fish and/or cephalopods identified as elephant fish (Callorhinchus callorynchus) (n = 6), E. maclovinus (n = 1), Enteroctopus megalocyathus (n = 1) and Doryteuthis sp. (n = 2). It is important to note that the regurgitation rate was probably underestimated because it may have occurred before sharks were being carried to the coast.
During the study, two juveniles (LT <190 cm) and one adult female of N. cepedianus were recaptured in the last fishing session on 21 January 2019, 2 km away from the original tagging site (location in Fig. 1). Total recapture rate was 3.4%, with two recaptures (164 and 198 cm LT at the moment of capture, and 170 and 210 cm LT at the moment of recapture, respectively) occurring 12 months after tagging and one (169 cm LT at the moment of capture and 172 cm LT at the moment of recapture) only five months after tagging.
Discussion
The two methodologies used to estimate relative abundance of sevengill sharks showed highest abundance during summer. However, spring surveys differed between the methods since catch and effort analysis suggests low abundance and BRUVS-derived indices indicated high abundance. This contradictory pattern pointed out the need of further sampling effort to better determine the time of arrival of sharks to the bay during warm months.
The near absence of sevengills in the outer portion of the bay as well as the low relative abundance in the mouth of the bay is significant. Furthermore, the shorter time of first occurrence recorded at the inner section of the bay suggests that sevengills aggregate specifically in this area. This short timing of occurrence also suggests that, at least in some occasions, BRUVS were deployed very close to the location of the sharks. These findings coincide with reports of local hookah divers (commercial algae harvest), who describe seeing schools of sharks ‘resting’ in the seafloor oriented against the current of the channel at the inner section of the bay (A. Irigoyen, unpubl. data, 2012).
The peak of both shark abundance and the occurrence of six spontaneous regurgitations (of a total of 12) with pieces of South American sea lion (O. flavescens) during late spring–summer coincided with the aggregation of the latter in breeding colonies (Campagna 1985), supporting the hypothesis that fluctuation in prey availability drives N. cepedianus seasonal patterns of abundance. By late summer, weanling pups perform their first swimming incursions when they become vulnerable to predation by sharks (Campagna 1985). Irigoyen et al. (2018) arrived to the same conclusion as they found that the peak of abundance of N. cepedianus coincided with the occurrence of regurgitated chunks of southern elephant seal (Mirounga leonina). Prey abundance is believed to be one of the main factors determining distribution of sharks (Speed et al. 2010; Schlaff et al. 2014).
All recaptures occurred inside the bay, suggesting that individuals were residents seasonally, possibly at the scale of months, and exhibited site fidelity between years. Similar results were obtained for N. cepedianus conventional tagging conducted in Caleta Valdés (Irigoyen et al. 2018) and Norfolk Bay (Barnett et al. 2010), where individuals were recorded repeatedly within a specific area. Evidence that recaptures in this work occurred at midday close to the central channel of the inner section of the bay, at close distance from the tagging site (near shore at high tide), suggests that sharks make nearshore incursions. Such incursions may be occurring in groups since captures and attacks to fishing lines happen typically on pulses, with more than one shark biting at the same time followed by extended intervals of no activity. Furthermore, the fact that the two sharks tagged on January 2018 and recaptured on January 2019 were caught and re-caught one after the other with minutes of difference in both occasions (9 and 4 min, respectively) suggests that sevengill sharks may move in cohesive groups. Further research on group behaviour must be conducted to address this question.
The present study allows for a more comprehensive understanding of the population structure of N. cepedianus in central Patagonia, possibly revealing the underlying spatial processes of the population. In Caleta Malaspina, juveniles were more frequent than adults, and adults did not show any evidence of mating scars or fluent claspers (i.e. not sexually active). This description of the population is similar to that found in a past study ~300 km southward in Ria Deseado (Cedrola et al. 2009). However, nearly 450 km northward of our study site (Caleta Valdés), adults dominated over juveniles and at least part of them were sexually active (Irigoyen et al. 2018). This comparison of studies suggests that juvenile N. cepedianus are capable to perform +700 km summer journeys to coastal foraging grounds that may act as distant secondary nurseries as pointed out by Cedrola et al. (2009). Further work is needed to comprehend the magnitude of the spatial ecology of N. cepedianus and its role within the Southwest Atlantic.
Acknowledgements
We specially thank anglers G. Zamora, M. Prado, G. Hunt and P. Panigutto; colleagues C. Awruch and C. Harillo; and Fundación TEMAIKEN for invaluable field support. We are grateful to A. Barnett for scientific advice. AJI, ADW and GAT were supported by the ‘Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)’. Shark Conservation Fund funded the study. Fieldwork included sampling within Interjurisdictional Marine Coastal Park Patagonia Austral and was authorised by the National Parks Agency (APN). Authors thank scientific and technological public policies conducted between 2003 and 2015 by the Argentinian government. Currently, the Argentinian science and technology system is close to collapse due to budget cuts. We urge the government of Argentina to revert these policies. The authors would like to thank two anonymous reviewers for their constructive comments on an early version of the manuscript.
