Size and sex composition of three carcharhiniform sharks landed by a coastal artisanal fleet from the northeastern coast of Brazil

Abstract Sharks are among the marine organisms most impacted by intense fisheries, a worrying fact since they are key components in the trophic structure of ecosystems. In this context, fish landing data can help managers in shark conservation. This study characterized the landings of Carcharhinus acronotus, Mustelus cf. canis, and Sphyrna mokarran in the Mucuripe Embayment, Ceará, Brazil, along three study periods (1998–1999, 2006–2008, and 2015–2016). A total of 223 specimens were recorded from 227 site visits. Carcharhinus acronotus specimens measured from 50 to 139 cm in total length (TL), with a 1.3:1 sex ratio in favor of males. Most of the specimens recorded were adults (55.1% of males and 62.9% of females). Mustelus cf. canis varied from 64 to 133 cm in TL, with a sex ratio in favor of females (3.1:1). Most of the specimens recorded were adults (50% of males and 68% of females). Sphyrna mokarran specimens varied from 116 to 380 cm in TL, with a sex ratio of 7:1 in favor of males. Most of the specimens recorded were juveniles. This is the first fishery-dependent study to provide information on size and sex composition of these species for most of the southwestern equatorial Atlantic.


INTRODUCTION
Some coastal and pelagic shark species are among the most overexploited groups of marine animals due to high fishing mortality, slow growth, late sexual maturation, and low fecundity (Holden, 1974;Cortés, 2000;Lucifora et al., 2011).This is worrying because they are key components in the trophic structure of tropical, subtropical and temperate areas (Ferretti et al., 2008(Ferretti et al., , 2010;;Navia et al., 2010;Bornatowski et al., 2014).Sharks are essential for marine ecosystems since they are top and mesopredators (Cortés, 1999;Rupp, Bornatowski, 2021) and the loss of the populations of these apex predators can significantly impact the trophic chain of marine ecosystems, affecting ecological processes and biogeochemical cycles (Estes et al., 2011), in addition to affecting the structure of coastal ecosystems (Ferretti et al., 2010).Therefore, evaluating and monitoring the population status of shark species is important for species conservation and, consequently, to the environment.Some factors such as the characteristics and variations of small-scale fisheries, in addition to sustainable fisheries management measures (closed fishing season, selectivity of fishing gear and others) were considered among the leading research priorities for conserving chondrichthyans in Latin America (Becerril-García et al., 2022).This information may become the basis for assessing stocks of these species and enabling the development of management plans later for overexploited shark species.
Despite the need to acknowledge basic biological aspects of sharks, there is a lack of information about the capture of sharks in several areas worldwide, and a complete lack of basic biological information in many areas, especially in the western equatorial Atlantic along the northeastern Brazil coast.It is estimated that the northeast region has about 40% of the fishermen's colonies distributed in 23 state federations in Brazil (Vasconcellos et al., 2007;Menezes et al., 2019).In this region, the Mucuripe Embayment, in Fortaleza, Ceará State, stands out as one of the main traditional fishery ports used to land and trade catches made by an artisanal fleet through multiple fishing gear (Aragão, Castro e Silva, 2006), being considered the main fishing point for comprising the largest artisanal fishing fleet in Fortaleza/Ceará (Menezes et al., 2019).Fisheries landings in the Mucuripe Embayment includes teleost fishes, crustaceans, mollusks, but sharks, and rays are also common (Faria et al., 2009;Santander-Neto et al., 2011a,b, 2020;Santander-Neto, Faria, 2020).Despite the knowledge about captured and landed elasmobranch diversity, there is a lack of information concerning their landings composition and population aspects (Santander-Neto et al., 2020).While the population structure of the nurse shark, Ginglymostoma cirratum (Bonnaterre, 1788) (Orectolobiformes) (Santander-Neto et al., 2011b) and blacktip shark, Carcharhinus limbatus (Valenciennes, 1839) (Santander-Neto et al., 2020) are already described for sharks landed by this fleet, the Carcharhinidae and Sphyrnidae families from the Carcharhiniformes order are among the groups with the least information available.For example, carcharhiniform species that lack such information are the blacknose, Carcharhinus acronotus (Poey, 1860), the hammerheads, Sphyrna spp., and the dusky smoothhound, Mustelus canis.
Given the need of knowledge about the basic biological aspects of carcharhiniform sharks in northeastern Brazil, the goal of the present study was to describe the landings composition of three carcharhiniform species caught and landed by a coastal artisanal fleet from northeastern Brazil: Carcharhinus acronotus, Mustelus canis and Sphyrna mokarran.This fishing area is located between the following coordinates: 03°43'S 38°05'W; 03°23'S 38°05'W and 03°25'S 38°48'W; 03°01'S 38°49'W (Fig. 1).Fisheries are conducted in depths ranging from 10 to 120 m.The fishing fleet is harbored in the Mucuripe Embayment, in Fortaleza.
The fishing fleet responsible for captures is mainly artisanal (small-scale).The vessels are motorboats (10 to 13 m in length) and fishing rafts (5 to 8 m in length).The motor boats remain from one to five days at sea, with an average of three days and the fishing rafts remain from three to six days at sea in depths ranging from 19 to 140 m (Freitas, 2020).Three fishing gears are used: (1) hook and line, which is composed of nylon line between 0.7 and 1 mm, hook size number 4 to 10 (up to 100 hooks are used in any given fishing trip); (2) longline, which is composed of nylon line of 2 mm and between 100 and 150 hooks with sizes varying from number 1 to 10; (3) surface and bottom gill-  nets, with mesh composed of nylon line with 0.5 to 0.9 mm, varying in the opening from 9 to 12 cm between opposite knots, each net having 100 m of longitudinal length and 4.8 m vertical length, around 100 nets being cast for each day of fishing.The hooks are used in "J" shape, usually for hook and line, and in circle hooks, usually used in longlines, or combined (Tab.1).
Field data.Three carcharhiniform species, blacknose, Carcharhinus acronotus, dusky smoothhound, Mustelus cf.canis, and great hammerhead, Sphyrna mokarran, landed by the Mucuripe Embayment fisheries fleet were recorded during three periods encompassing a time span of around 20 years.Study period 1 extended from May/1998 to April/1999.Study period 2 extended from November/2006 to October /2008.Study period 3 extended from August/2015 to July/2016.The site visits were conducted weekly.All the individuals landed and available for trade were sexed and measured for Total Length in straight-line (TL; in cm) using a tape measure.Species identification followed Compagno (1984), Gadig (2001), Rosa (2009), Gomes et al. (2010), and Rosa, Gadig (2010).Due to the dynamics associated to a fish landing port, since all sharks are sold, and taking into consideration taxonomic difficulties involving the identification smoothhound sharks (Bigelow, Schroeder, 1940;Heemstra, 1997), all individuals identified as Mustelus canis at the landing site were referred as Mustelus cf.canis in the present study.Animal welfare laws, guidelines or policies were not applicable because no live fish was sampled/captured or collected during the present study, which was based on landed specimens being sold to the public by fishermen.Data analysis.The three species were characterized for: (1) total number of specimens landed; (2) minimum, maximum, and average total length (TL); (3) sexual proportion; and (4) number of specimens per study period.In addition, the most abundant species, C. acronotus, was also characterized for monthly variations on the number of specimens recorded.
The maturity proportion was also characterized for all three species.The specimens were classified as 'juveniles' or 'adults' based on their TL, following the smaller mature individuals for each species described in the literature.Carcharhinus acronotus matures at 103 (female) and 104 (male) cm (Hazin et al., 2002).Mustelus cf.canis matures at 97 (female) and 81 (male) cm (Conrath, Musick, 2002).Sphyrna mokarran matures between 210 and 237 cm (female) and between 217 and 227 cm (male) (Stevens, Lyle, 1989;Cliff, 1995;Harry et al., 2011a).The distribution of TL classes was determined for each species.This provided a graphic depiction of the occurrence of juveniles and adult specimens in the landings.Size and sex composition of three shark species Statistical analyses.Normality tests were applied to each dataset of 'male/female TL' and 'number of landed specimens per study period' before statistical analyses.Two tests were performed with this purpose: the Kolmogorov-Smirnov test when sample sizes were greater than 50 (α = 0.05) and the Shapiro-Wilk test when sample sizes were smaller than 50 (α = 0.05).To test for homoscedasticity, the male/female TL dataset was submitted to the F-Test to compare two variances (α = 0.05).The Bartlett's Test was applied for the number of landed specimens per study period to verify if variances were equal across the three periods (α = 0.05).The dataset was log-transformed when the assumption of normality and homoscedasticity was not met.Then, the non-parametric tests described below in each subsection were applied, as recommended by Zar (2010).
Differences in the sex ratio of males and females were tested using the chi-square test.Differences in TL between sexes were tested for the most abundant species, C. acronotus and M. cf.canis, through the non-parametric Student's t-test (Wilcoxon-Mann-Whitney, α = 0.05) (Zar, 2010).
The most abundant species, C. acronotus and M. cf.canis, were tested to identify any sign of changes for their landings composition between three periods.All specimens (i.e., juveniles and adults) were considered for calculating each period's number of individuals landed.The statistical significance of each comparison was tested using Kruskal-Wallis (α = 0.05).In cases where significant differences were detected, a procedure for multiple post hoc comparisons was adopted (Nemenyi Test) (Tabs.S1, S2 and S3).The statistical analyses were performed using the software R v. 3.3.3 (R Development Core Team, 2018).

RESULTS
A total of 223 individuals of three carcharhiniform sharks, Carcharhinus acronotus, Mustelus cf.canis, and Sphyrna mokarran, were recorded from 227 site visits (Tab.2).Carcharhinus acronotus.A total of 140 individuals were recorded, resulting in an approximate rate of one specimen per two days of site visits.These specimens varied between 50 and 139 cm in total length (TL).Most specimens (25%) measured from 120 to 130 cm TL, while 12% of them measured from 130 to 140 cm TL.The average TL for males was 99.7 ± 25.7 cm and the average TL for females was 106.6 ± 27.3 cm.Overall, females were larger than males in TL (W = 2949.5;p = 0.026).About their sex, 78 specimens were males and 62 were females, which resulted in a 1.3:1 sex ratio that was not significantly different from the expected ratio of 1:1 (x² = 1.829; p = 0.2049, GL = 1).Most of the specimens recorded were adults (55.1% of males and 62.9% of females) (Fig. 2A).The number of specimens recorded differed (KW = 6.303; p = 0.042, GL = 2) along the study periods [90 individuals for period 1 (64%), 45 for period 2 (32%), and 5 for period 3 (4%)] (Tab.2; Fig. 3).For periods 1 and 2, 57 individuals were juveniles (42.2%) and 78 were adults (57.8%).For period 3, only one juvenile and four adults were recorded and several TL classes of C. acronotus were not recorded in landings during this period (Fig. 3A).Regardless of study period and considering landings per month of any given year, juveniles (75.9%) were mostly recorded between December and March, while adults (62.19%) were mostly recorded for April, July, August, and November.

Species
Mustelus cf.canis.A total of 67 specimens were recorded on landings, resulting in a rate of one specimen per three days of site visits.These specimens varied from 64 to 133 cm in TL.Most specimens (22%) measured from 110 to 120 cm in TL (Fig. 2B).The average TL for males was 82.3 ± 13.2 cm and the average TL for females was 101.2 ± 17.8 cm.Overall, females were larger than males in TL (W = 657; p = 0.0008).About their sex, 66 out of the 67 recorded specimens were sexed, in which 50 were females and 16 were males, which resulted in a sex ratio of 3.1:1.This pattern in the sex ratio of females and males was significantly different (x² = 17.515; p < 0.0001, GL = 1).Most of the specimens recorded were adults (50% of males and 68% of females) (Fig. 2B).The number of specimens recorded in landings did not significantly differ among the three study periods (KW = 3.530; p = 0.171, GL = 2) [4 specimens (6%) in period 1, 54 in period 2 (81%), and 9 in period 3 (13%)] (Tab.2; Fig. 3).Sphyrna mokarran.A total of 16 specimens were recorded in landings, resulting in a rate of approximately one specimen per 14 days of site visits.These specimens varied from 116 to 380 cm in TL, with the modal class of 160-210 cm being the most representative among the individuals sampled (31% of the individuals) (Fig. 2C).The average TL for males was 197.4 ± 55.1 cm and the average TL for females was 330 ± 70.7 cm.These were 14 males and two females, which resulted in a sex ratio of 7:1 that was significantly different from the expected ratio of 1:1 (p = 0.006).Most of the specimens recorded were juveniles (nine of the 14 males representing 64.3%) (Fig. 2C).As for the only two females recorded, they were 280 and 380 cm in TL (the latter carrying 34 embryos).The distribution of specimens per study period was as follows: 3 specimens for period 1 (19%), 6 for period 2 (37%), and 7 for period 3 (44%).

DISCUSSION
This is the first fishery-dependent study to provide information on size and sex composition of Carcharhinus acronotus, Mustelus cf.canis, and Sphyrna mokarran landed by any fishing fleet for most of the southwestern equatorial Atlantic.The data obtained in the present study does not allow inferences on species abundance, since it lacks fishing effort data.But it is an improvement on the knowledge about shark landings in the region.This is because information such as number of individuals landed, total length, sexual proportion and others are under the research priorities for conserving the chondrichthyans in Latin America (Becerril-García et al., 2022).Local data are crucial for management and conservation of aquatic organisms since they can serve for the establishment of management approaches (Carr, Heyman, 2016).This kind of information is also especially important because no official fisheries statistics has been collected in Brazil for over a decade already (Gonçalves-Neto et al., 2021).Besides, lack of data with enough taxonomic resolution also prevents any use of traditional models based on catch per unit of effort in stock assessments (Dulvy et al., 2014).
Shark fisheries developed in the northeast region seem to follow the same pattern regarding the use of fishing gear.The Mucuripe Embayment fleet uses multiple fishing gears to capture sharks, following the same pattern used in other fisheries developed in the northeast region (Lessa, 1986a,b;Hazin et al., 2002;Meneses et al., 2005;Yokota, Lessa, 2006;Fischer et al., 2009;Afonso et al., 2011;Barreto et al., 2011;Zagaglia et al., 2011).The Mucuripe Embayment fleet fishes both in distant areas and near the coast, with a stable fishing effort over the years, mainly due to the constant use of rafts and motorboats, such as fishing vessels, and gill nets, hook and lines and longlines, as fishing gear (Menezes et al., 2019).In addition to the use of longlines to capture sharks, it should be noted that it is common for these individuals to be captured by gill nets and hook and lines as by-catch fauna of other types of fishing resources captured and landed by this fleet.Size and sex composition of three shark species A large part of these fish landings in Ceará State originate from artisanal fisheries.The artisanal vessels represent over 70% of the maritime fishing fleet and are responsible for more than half of all fish production landed on the Ceará coast (Brasil, 2002), demonstrating their great capacity for capturing several species.The elasmobranch fauna landed at the Mucuripe Embayment has been studied in the recent years (Faria et al., 2009;Santander-Neto et al., 2011a,b, 2020, 2022;Santander-Neto, Faria, 2020), where there was little variation in the fishing gears used in the fisheries.This fleet trade sharks without distinction of species, considering only the size of individuals as a price differential.

Carcharhinus acronotus.
The discussion about the biology, fisheries and conservation of blacknose is essential to clarify its life history and assess the fishing pressure exerted on this species.Carcharhinus acronotus has relatively high fishing mortality (80% mortality rate; Afonso et al., 2014), it is susceptible to several fishing gears and captured primarily as a bycatch along its distribution range (Nichols, 2007;Barreto et al., 2011).As a coastal species, it is inevitably vulnerable to gill-net fisheries (Trent et al., 1997).Furthermore, different populations of C. acronotus seem to show regional differences between the life history parameters (L∞, k, longevity) along their distribution (Driggers et al., 2004), corroborating the need for fisheries data that can support management initiatives related to C. acronotus as separate stocks.
The sex ratio indicated a greater number of males than females in fishing landings but was not significantly different from the expected ratio of 1:1.This pattern differed from the capture pattern of individuals of this species in Pernambuco, Brazil (Hazin et al., 2002;Barreto et al., 2011), where a greater number of females were captured compared to males.The variation in this study may be related to the seasonal pattern of females that seem to move away from coastal waters during specific periods of the year (Afonso et al., 2014).
Both juvenile and adult blacknose used to be caught and landed by the studied local fleet, but juveniles were not recorded in the last of the three studied periods.Blacknose juveniles occur mainly in coastal waters (Afonso et al., 2014) and are caught by fisheries in other parts of northeastern Brazil (Barreto et al., 2011).Being a coastal species, C. acronotus can be captured by several fishing devices and all length classes are vulnerable once the Mucuripe Embayment fleet also deploys its fishing gears in shallow waters (Freitas, 2020).All length classes were recorded during the first two periods, but this pattern changed in the third study period when fewer adults were recorded, and the lower-length classes were no longer recorded.Since fishing effort data is lacking, it is not known if this pattern reflects a change in local relative abundance or any change that might have occurred in the fishing fleet or fishing effort in the past years.For instance, selectivity of the hooks was considered one potential cause for the low number of juveniles recorded for coastal waters of Pernambuco State, also in northeastern Brazil (Afonso et al., 2014).On the other hand, declines in captures of C. acronotus have already been detected in other parts of coastal northeastern Brazil (Pernambuco; Afonso et al., 2014) and southern USA (Florida;Siegfried, Brooks, 2007).Therefore, further assessments that include fishing effort data are needed to better clarify the difference in the number of individuals landed over time detected in the present study.
Mustelus cf.canis.The fisheries in the region capture mainly adults, notably females, which are larger than males in fishing landings at Mucuripe Embayment.This distribution for the species was also observed on the north atlantic coast of the United States (Dell'Apa et al., 2018) and in northeastern coast of Brazil (Zagaglia et al., 2011) and may be related to the behavior of females that inhabit shallow inshore coastal waters compared to adult males that appear to have a seasonal pattern in their occurrence (Dell'Aapa et al., 2018).
The higher frequency of females in coastal waters can be directly related to the number of juveniles.In an estuary in the south of New Jersey, 96% of juveniles of the year of M. canis were caught by a variety of fishing gear (Rountree, Able, 1996).The predominance of juveniles in coastal waters shown in this study has also been described for other shark species in northeastern Brazil (Lessa, 1986a;Lessa, Almeida, 1997;Yokota, Lessa, 2006;Lessa et al., 2016).This pattern has also already been detected for the nurse shark, Ginglymostoma cirratum, and blacktip shark, Carcharhinus limbatus, captured by this same fishing fleet (Santander-Neto et al., 2011b, 2020).
The landings of M. cf.canis in the area did not differ between periods.As already mentioned, the lack of fishing effort data in this study prevents inferring any population trend.However, it is important to emphasize the relatively lower susceptibility of this species to fishing pressure.Mustelus canis grows quicker and reaches sexual maturity at a younger age in comparison to other shark species as for example M. lenticulatus Phillipps, 1932, M. antarticus Günther, 1870, M. henlei (Gill, 1863), M. californicus Gill, 1864, Carcharhinus obscurus (Lesueur, 1818), Rhizoprionodon taylori (Ogilby, 1915) (Conrath et al., 2002), which likely provides more productivity and resistance to fisheries exploitation (Conrath et al., 2002).A previous data on fisheries for this species in Ceará, where 154 specimens were captured between 1997 and 2001 using bottom longlines between 100 and 350 m with a capture per unit of effort (CPUE) of 0.18 individuals per 100 hooks, considered the population of this species as "sustainable" for those years (Brasil, 2006).
Sphyrna mokarran.The low frequency of observed landings suggests that the captures of the great hammerhead by the Mucuripe artisanal fishing fleet are accidental or eventual.The broad variation in length classes from sampled individuals (116-380 cm) is likely related to gears used by the studied fishing fleet, which includes fishing gears specific to capture large sharks (longlines) and other types of fishing gears including nets that capture other mesopredator sharks as bycatch.Besides gear selectivity, it is not known if catches of this species in the past had any major impact on its population, leading to the low numbers recorded nowadays in the landings once this species has high vulnerability to fishing pressure (Rosa et al., 2018).Sphyrna mokarran is experiencing population declines worldwide (Rigby et al., 2019), including South Africa (Cliff, 1995;Gullak et al., 2015), Indian Ocean, Northwest Atlantic, and Gulf of Mexico (Rigby et al., 2019).Some factors emphasize the vulnerability of the species to fishing, such as the high value and trade of its fins (Rigby et al., 2019;Cardeñosa et al., 2020), their easy catch in coastal regions by commercial pelagic fisheries (Calich, 2016), and due to their relevance for sport fishing (Shiffman, Hammerschlag, 2014).
The landings of S. mokarran by the Mucuripe fleet are primarily composed of juvenile males, a typical capture pattern for the species.World records indicate a larger number of juveniles, primarily males, in South Africa (Cliff, 1995) and in coral reef areas in Australia (Harry et al., 2011b), indicating that juvenile individuals are more susceptible .br | scielo.br/niSize and sex composition of three shark species MATERIAL AND METHODS Fisheries area and fleet.The carcharhiniform sharks examined in the present study were captured on the northeastern coast of Brazil.More specifically, the fishing area extends along the Ceará Basin, from Paracuru to Aquiraz (central coast of Ceará State).

FIGURE 1 |
FIGURE 1 | Operational area of the artisanal fishing fleet based in the Mucuripe Embayment, Fortaleza, Ceará (delimited by dotted lines).Bathymetric curves and the municipalities' location on the Ceará coast are indicated as additional references to the limit of the fleet operation in the study area, highlighting the Ceará State.

TABLE 1 |
Fishing gears used to capture the sharks landed in Mucuripe Embayment.

TABLE 2 |
Summary of the number of individuals (N) and days of sampling by species and sampling period.7/18 ni.bio.br| scielo.br/niWaslley M. Pinheiro, Jones Santander-Neto, Isabelle D. B. Arthaud and Vicente V. Faria