Catch Composition, Seasonality, and Biological Aspects of Sharks Caught in the Ecuadorian Paciﬁc

: Although sharks have a fundamental role in maintaining the balance of aquatic ecosystems, exerting a great inﬂuence on lower levels of the food chain, their populations are declining worldwide due, to a large extent, to overﬁshing. Of the 64 species registered in Ecuador, from January to December 2019, 19 species were recorded in Manta from the 15,455 captured individuals, with the family Carcharhinidae being the most abundant in the catches (69.4%), and the most abundant species was Prionace glauca (57.9%). Regarding threatened species, such as Carcharhinus longimanus , Sphyrna lewini , and Sphyrna zygaena , a greater presence of immature specimens was observed in landings. However, information on the composition and biological aspects of shark species in the Ecuadorian Paciﬁc is very scarce. Therefore, research on the characteristics of life history (age, growth, and maturity) are of utmost importance for the stock assessments that are being exploited, especially in developing countries, where this information is lacking, causing inadequate management of ﬁshery resources.


Introduction
Sharks have a fundamental role in maintaining the balance of aquatic ecosystems because, being at higher trophic levels, they can exert a great influence on lower levels [1].However, they are currently declining worldwide due to overfishing, habitat degradation, climate change, and pollution [2][3][4][5].This decrease is intensified by their biological characteristics, such as slow growth, late maturity, and few offspring [6].Regional information on shark catches is essential to be able to know the patterns of catches at a global level [7].Likewise, research on life history characteristics (age, growth, and maturity) is very important for the stock assessments that are being developed [8].However, in developing countries this information is very scarce [9,10].This lack of information can lead to the use of information from other regions, causing an inadequate management of fishery resources [11,12].
According to the FAO [13], in South America from 1950 to 2020, 4,133,991 live-weight tons of cartilaginous fish were reported.In Peru, González-Pestana et al. [14] reported that 6099 tons (t) of sharks were landed per year from 1950 to 2010.The most abundant species in Peruvian waters were Prionace glauca, Isurus oxyrinchus, and Sphyrna zygaena.In the Ecuadorian Pacific, Jacquet et al. [15] estimated that 7000 tons of sharks were landed per year from 1979 to 2004.About 119 species of cartilaginous fish have been recorded in Ecuador, of which 64 correspond to sharks [16].The most frequently landed shark species in the Ecuadorian Pacific are Alopias pelagicus, P. glauca and Carcharhinus falciformis [17].The main ports where sharks are landed in Ecuador are Manta, Santa Rosa, Esmeraldas, Anconcito, Puerto López and Puerto Bolívar.Manta is the port with the highest number of shark landings [18].In addition, during the dry season (April-November), this port presents the highest number of shark catches [17].Information on the composition of species and some biological aspects in the Ecuadorian Pacific is very scarce and dates back more than 10 years [17][18][19][20][21].Therefore, the objective of this study is to update the information on the species composition, seasonality, size structures, sexual proportion, morphometric relationships, and sexual maturity size in Ecuadorian waters.

Materials and Methods
From January to December of 2019, field trips were conducted to the "Playita mía" pier in Manta (0 • 56 59 S, 80 • 42 34 W).The visits were daily throughout the year with the objective of having a good sampling effort.Sharks were landed gutted with all fins, and were accurately identified at a species level by using the guide of Martínez-Ortiz and García-Domínguez [22].The landed organisms were sexed and measured with a measuring tape graduated in centimeters (cm).The measurements taken were total length (TL), precaudal length (PCL), and interdorsal length (IL).In males, clasper length (CL) was measured from the point of rotation to the tip of the copulatory apparatus.In addition, clasper characteristics such as rotation, noncalcification, semicalcification, total calcification, rhipidion aperture, and absence or presence of sperm were recorded [23][24][25].
Like other studies [26][27][28], weight was estimated from TL by using the following potential equation, where W is the weight, a is the intercept and b the slope.The values of these parameters for each shark species recorded in this study were obtained from previous ones as shown in Table 1.
For the adjustment of a logistic model to the binomial maturity data (0, immature; 1, mature), categories 0, non-calcified, and 1, semi-calcified, were grouped as immature and category 2, calcified, as mature.Maturity size for males was estimated by using the following equation [29], where P max is the maximum proportion of mature specimens, l 50 and l 95 correspond to the length at which 50% and 95% of individuals have reached sexual maturity, respectively.The inflexion point was estimated by using the following equation [30], where a is the inflexion point, CL max and CL min are the maximum and minimum clasper lengths, respectively.The inflexion point was only estimated when the data were adjusted to the logistic function [31,32].The lengths of the most abundant species (n ≥ 20) were plotted in frequency histograms.If the data met the normality and homoscedasticity assumptions, the student's ttest was performed, otherwise, the Mann-Whitney U-test was performed, to know whether there were differences between average lengths of sexes.The chi-square test (χ 2 ) was also performed to determine whether the sexual ratio was significantly different with respect to the expected 1:1 ratio [33].

Family Alopiidae
The biological aspects of A. pelagicus and A. superciliosus were previously published by Briones-Mendoza et al. (see [56]).

Composition of Catches
Approximately 64 shark species have been reported in Ecuador [16].Between 2003 and 2006, Martínez-Ortíz et al. [17] documented 34 species of sharks in Manta.However, only 19 species were recorded in this study.This could be possibly due to the fact that the sampling in this study was only for one year, whereas that of Martínez-Ortíz et al. covered 3 years, although a possible loss of diversity as a result of increased fishing effort should not be discarded [7,57,58].Sixteen years ago, Martínez-Ortíz et al. reported that the dominant species in landings in Manta was A. pelagicus, representing the 36% of the total species landed.However, in this study a decrease of 15.7% was observed, and Prionace glauca has become the dominant species in landings in Manta, with an increase of 33.9% (Figure 6).It is possible that these changes are due to overfishing and differences in the life history characteristics of both species.For example, P. glauca has an average of 30 offspring per litter [59], whereas A. pelagicus has only 2 offspring per litter [39].C. falciformis remains in third place.However, it has suffered a decrease of 4.8%.In the case of vulnerable species, such as S. zygaena [60], and a critically endangered species, such as S. lewini [61], a decrease in landings is reported [17] (Figure 6).It is possible that this was related to the implementation of Ministerial Agreement 116, which allows Ecuadorian artisanal vessels to hold on board as bycatch a maximum of five hammerhead shark (juveniles up to 150 cm LT), which must have their fins attached to the body [62].The season of greatest shark landings was the dry season (April-November).This could be due to 2 reasons, according to Martínez-Ortíz et al. [17].First, the different type of fishing material and depth at which the hooks operate during the dry and rainy (December-March) seasons.Second, directed fishing at sharks due to the low abundance of target species during the dry season.
In this study, two demersal species (Squatina californica and M. lunulatus) and 17 pelagic species were reported.This could be due to the fact that in Manta the dominant fishing gear is the pelagic longline, representing 82% of the landings [63].There are two very well-defined fishing seasons in Ecuador.The first goes from May to November and is characterized by directed fishing for tuna, swordfish, and billfish, where fishermen use circle hooks number 36 and 38.The second is distinguished by directed fishing for Coryphaena hippurus that goes from December to April and uses J hooks number 4 and 5. Artisanal vessels that use pelagic longlines generally fish between 20 and 70 nm off the coast [64].This study does not provide detailed information regarding the gear and fishing method used, which must be well understood before developing a fishery management strategy [26].Therefore, in future research, this information should be better documented to improve fishery-management strategies.The size range (61-272 cm TL) reported in this study was lower than that recorded in Manta, between 2003 and 2006 (61-309 cm TL) [17], in Campeche Bank, between 1985 and 1989 (65-314 cm TL) [65], and that the maximum size recorded in the annotated checklist of the chondrichthyan fishes (350 cm TL) by Weigmann (2016) [66].However, the size range of this study closely resembles the one reported in the central-western Pacific in 2014 (65-271 cm TL) [11].The sex ratio was skewed toward females, which coincides with what was reported by Hoyos-Padilla et al. [67] and Varghese et al. [68].However, it differs from other studies [17,69,70], which found no difference in abundance between females and males.The size at maturity for males was 182.38 cm TL, which was very similar to that recorded in the central-western Pacific (183 cm TL) [11], in the Mexican South Pacific (180 cm TL) [69] and on the west coast of Baja California Sur (182 cm TL) [67].However, the size at maturity seems to be bigger in the eastern Indian Ocean (207.6 cm TL) [70], in the eastern Arabian Sea (218.98 cm TL) [68], and in Campeche Bank (225 cm TL) [65].These results suggest that males of C. falciformis reach sexual maturity at a smaller size in the Pacific Ocean.The estimated inflexion point in the eastern Indian Ocean was at 196.9 cm TL [70], which appears to be above the one reported by this study for the Ecuadorian Pacific (188.5 cm TL).

Carcharhinus longimanus
The maximum length recorded in this study (215 cm TL) for C. longimanus was lower than other lengths reported in previous studies [71][72][73][74] and than that documented in the annotated checklist of the chondrichthyan fishes (350 cm TL) [66].As reported in other papers [42,74], no significant differences in sex ratio were found in this study.In the western Central Pacific Ocean, D'Alberto et al. [75] reported that the smallest mature male of C. longimanus averages 190 cm TL, whereas the larger immature one was 195 cm TL.In the western North Pacific Ocean, Joung et al. [42] found that the smallest mature male averaged 172 cm TL, whereas the larger immature averaged 202 cm TL.In this study, only one mature individual was found, which averages 175 cm TL, and the largest immature male measured 185 cm TL.It was estimated that 94% of C. longimanus examined males had not reached sexual maturity, whereas all females were immature, taking as a reference the maturity length estimated by D'Alberto et al. (224 cm TL) [75].Due to this fact, it is possible that females of C. longimanus approach coastal areas to give birth to their young [76], which would facilitate the capture of juvenile specimens [77].Therefore, these results suggest possible breeding areas for C. longimanus in Ecuadorian waters.

Prionace glauca
The maximum size of P. glauca (314 cm TL) is similar to the one reported by other studies [78][79][80][81] and less than that recorded globally (383.5 cm TL) [66].However, the minimum size was larger than that documented in Mexican waters [77,82].This is likely due to the breeding areas found in the Mexican Pacific [83].The sex ratio was skewed toward females in this study, which is consistent with data reported by Cruz-Ramírez et al. [82].However, Carrera-Fernández et al. [77] found a biased proportion toward males, whereas other studies found no difference in abundance between females and males [78,84].The average maturity size was 192.88 cm TL, which is similar to that recorded in the southeastern Pacific Ocean (190.3 cm TL) [84], in the Ecuadorian Pacific (187.1 cm TL) [78], although compared to northeastern Brazil, higher values have been reported in this study (225 cm TL) [81].However, da Silva et al. [85], in one review, found no difference in the mean size at maturity of the studies among oceans.

Isurus oxyrinchus
This present study reported a greater size range (83-341 cm TL) than the ones performed in eastern Indonesia (130.8-310cm TL) [86], in the eastern Arabian Sea (97-269 cm TL) [68], and in the southeastern Pacific Ocean (75.5-240 cm TL) [84].However, it was lower than the northwest Pacific (80-375 cm TL) [47] and the maximum size reported globally (445 cm TL) [66].No differences in sex ratio from expected were found, which is consistent with other studies [68,84,87,88], although other ones have shown bias toward males [89] and females [90].The size at maturity for males was estimated at 194.52 cm TL, which is similar to that reported in New South Wales, Australia (195 cm TL) [87] and South Africa (194-206 cm TL) [91].However, in the northwest Pacific, a larger length at maturity (210.2 cm TL) was recorded [47], whereas in eastern Indonesia (185.7 cm TL) [86], on the southwest coast of Baja California (180 cm TL) [88] and in the southeastern Pacific Ocean (180.2 cm TL) the sizes at maturity were smaller than those reported in this present study for the Ecuadorian Pacific.The estimated inflexion point in this study (178.82cm TL) was higher than that of eastern Indonesia (164.8 cm TL) [86].

Pseudocarcharias kamoharai
In the Ecuadorian Pacific, between 2003 and 2009, a maximum length of 113 cm TL was reported [92], which coincides with the value reported in this present study (114 cm TL).However, it was lower than the recorded length in the southwest Atlantic Ocean (122 cm TL) [93] and that the maximum size worldwide (122 cm TL) [66].In this study, the sex ratio was not significantly different from the expected 1:1, which differs from some studies that found a sex ratio skewed towards females [86,92,93] and males [94,95].The sexual maturity size recorded for the Ecuadorian Pacific was 80.52 cm TL, which is quite similar to the ones registered in the same area between 2003 and 2009 (78.9 cm TL) [92] and in the southwest Atlantic Ocean, between 2005 and 2007 (80 cm TL) [93].However, the size at maturity of this study was higher than the one reported in eastern Indonesia (72.5 cm TL) [86] and lower than that recorded in the eastern tropical Atlantic (89.4 cm TL) [96].

Sphyrna lewini
The maximum length recorded in this study (276 cm TL) was smaller than that observed in the Ecuadorian Pacific, between 2003 and 2009 (310 cm TL) [97], in the Gulf of California (363 cm TL) [98], in Indonesian waters (316.8 cm TL) [99], in northeastern Brazil (321 cm TL) [100], and all over the world (430 cm TL) [66].It is possible that this is due to the fact that in Ecuador only the incidental capture of a maximum of five individuals with a size less than 150 cm TL is allowed, according to Ministerial Agreement 116 [62].However, in this study five specimens of S. lewini exceeding 150 cm TL were reported.The sex ratio was significantly different from parity, which coincides with that reported in Ecuadorian Pacific, where a sex ratio biased toward females was recorded [97], but differs from that reported in Indonesian waters [99], where they found no differences in sex ratio.All males reported in this study were immature, as they did not have fully calcified claspers.Taking as a reference the size at maturity for females reported by Estupiñán-Montaño et al. in the Ecuadorian Pacific (219.4 cm TL) [97], 88.9% (n = 8) of the females reported in this study were immature, whereas only 11.1% (n = 1) were mature.These results coincide with those documented by Estupiñán-Montaño et al. [97], who also found a greater presence of immature specimens in landings, suggesting possible breeding areas.

Sphyrna zygaena
As mentioned before, it is forbidden to catch specimens of hammerhead sharks greater than 150 cm TL in Ecuador.However, this study recorded 38 specimens of S. zygaena with sizes exceeding 150 cm TL.Therefore, a greater vigilance and the application of stricter laws are needed [101,102].Regarding the sex ratio, no significant differences from expected were found, disagreeing with what was reported in the Ecuadorian Pacific between 2003 and 2006, where the sex ratio was biased toward males [17], whereas another study carried out between 2007 and 2012 in the same region registered bias toward females [103].The size at maturity for males in this study (200.81cm TL) was larger than that reported in the Gulf of California, between 1995 and 2000 (193.7 cm TL) [48], but smaller than the one reported in the Ecuadorian Pacific between 2003 and 2006 (215 cm TL) [104] and between 2007 and 2012 (263.7 cm TL) [103].According to the size at maturity of this study, 89.80% of the landed male individuals were immature, whereas 97.67% of the females had not reached sexual maturity, taking as a reference the maturity size estimated by López-Martínez et al. (239.3 cm TL) [103].These results are consistent with other studies conducted in the Ecuadorian Pacific [18,21], where most of the individuals landed were immature.The concordances in the results of these studies seem to be associated with the fact that S. zygaena remains in coastal areas during the first years of life [76,105] and, therefore, is more susceptible to capture.

Mustelus lunulatus
The size range reported in this work (49-123 cm TL) was very similar to that documented in the Colombian Pacific in 2001 (50-125 cm TL) [106], but in the Ecuadorian Pacific the size range was wider in 2013 (41.4-135 cm TL) [107] and was also less than the maximum length recorded by Weigmann (2016) in the annotated checklist of the chondrichthyan fishes (175 cm TL) [66].Females were significantly more abundant than males, disagreeing with what was documented in Colombia [106] and Ecuador [107], where the sexual proportion was no different from parity.The length at maturity for males (95.93 cm TL) was similar to that reported in the Gulf of California (91.5 cm TL) [108] and in the Ecuadorian Pacific (97.2 cm TL) [107].Of the total number of males examined, 75% were immature.As for females, 82% had not reached sexual maturity, according to the maturity size estimated by Pérez-Jiménez and Sosa-Nishizaki (103.2 cm TL) [108].These results coincide with those reported by other studies [106][107][108], which also recorded a greater number of immature individuals.
In this study, a decrease in the relative abundance of some species of great commercial interest such as A. pelagicus, C. falciformis, S. zygaena, and S. lewini was found.Nevertheless, research on life history characteristics (age, growth, and maturity) of sharks in the Ecuadorian Pacific is very scarce and outdated.This information is essential to carry out stock assessments that are being exploited.Therefore, it is recommended to carry out studies to fill the information gaps that exist in this area and thereby improve the management of sharks in Ecuador.

Figure 5 .
Figure 5. Length at maturity of male individuals of the main shark species landed in Manta: (a) Carcharhinus falciformis; (b) Prionace glauca; (c) Isurus oxyrinchus; (d) Pseudocarcharias kamoharai; (e) Sphyrna zygaena; (f) Mustelus lunulatus.The black dots in the middle of the curve correspond to the length at which 50% of individuals have reached sexual maturity (TL 50 ).The black dots at the top and bottom correspond to mature and immature individuals, respectively.The purple shaded areas represent the 95% bootstrapped confidence intervals.

Figure 6 .
Figure 6.Comparison of changes in landings of the shark species most frequently landed in Manta [17].

Table 1 .
Parameters used to estimate the weight from the length of the sharks landed in the Ecuadorian Pacific.

Table 3 .
Descriptive statistics of shark species measured during the year 2019 in Manta.The meaning of the abbreviations of the categories of the Red List of

Table 4 .
Monthly sex ratios of the main species landed in the Ecuadorian Pacific.