Size at Sexual Maturity of Deep-Sea Unexploited Caribbean Metanephrops binghami (Boone, 1927) and Overexploited Mediterranean Nephrops norvegicus (Linnaeus, 1758) Using Morphometric and Gonadal Staging Approaches

Citation: Paramo, J.; Rodriguez, A.; Zabala, J.Q.; Company, J.B.; Pérez, D.; Vigo, M.; Santos-Bethencourt, R.; Aguzzi, J.; Bahamon, N. Size at Sexual Maturity of Deep-Sea Unexploited Caribbean Metanephrops binghami (Boone, 1927) and Overexploited Mediterranean Nephrops norvegicus (Linnaeus, 1758) Using Morphometric and Gonadal Staging Approaches. Fishes 2024,9, 78. https://doi.org/ 10.3390/fishes9030078 Academic Editor: Alberto Teodorico Correia Received: 19 December 2023 Revised: 11 February 2024 Accepted: 16 February 2024 Published: 20 February 2024 Copyright: © 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). fishes Article Size at Sexual Maturity of Deep-Sea Unexploited Caribbean Metanephrops binghami (Boone, 1927) and Overexploited Mediterranean Nephrops norvegicus (Linnaeus, 1758) Using Morphometric and Gonadal Staging Approaches Jorge Paramo 1,* , Alfredo Rodriguez 1,2 , Juliana Quevedo Zabala 3, Joan B. Company 3,4 , Daniel Pérez 2,5 , Maria Vigo 3, Ricardo Santos-Bethencourt 3,4, Jacopo Aguzzi 3and Nixon Bahamon 3 1Tropical Fisheries Science and Technology Research Group (CITEPT), University of Magdalena, Santa Marta 470004, Colombia; [email protected] 2Doctoral Program in Marine Sciences, University of Magdalena, Santa Marta 470004, Colombia; [email protected] 3Institut de Ciències del Mar (ICM-CSIC), 08003 Barcelona, Spain; [email protected] (J.Q.Z.); [email protected] (J.B.C.); [email protected] (M.V.); [email protected] (R.S.-B.); [email protected] (J.A.); [email protected] (N.B.) 4Institut Catalàde Recerca per a la Governança del Mar (ICATMAR), 08003 Barcelona, Spain 5Programa Biología Marina, Facultad de Ciencias Naturales e Ingeniería, Universidad de BogotáJorge Tadeo Lozano, Santa Marta 470004, Colombia *Correspondence: [email protected] Abstract: The deep-sea Caribbean lobster (Metanephrops binghami) and the Norway lobster (Nephrops norvegicus) are Nephropidae species of high commercial interest. Although the first one still remains unexploited, the second is overexploited in the Mediterranean Sea. For effective fisheries management, size at sexual maturity is an essential indicator to protect immature individuals from exploitation. The estimation of this indicator can, however, be biased due to the difficulty of differentiating juveniles from adults by their size structure due to the natural process of molting. This study aims to estimate the size at sexual maturity of M. binghami and N. norvegicus females by comparing the effectiveness of the morphometric method versus the macroscopic evaluation of gonad maturity. Samples of M. binghami were collected from the Colombian Caribbean Sea in August and December 2009, March and May 2010, and August 2020 to May 2021. Samples of N. norvegicus were collected from the northwestern Mediterranean Sea from 2019 to 2022. Similar sizes at sexual maturity were found for M. binghami between the morphometric approach (ranging from 28.6 to 33.9 mm cephalothorax length, CL) and the gonadal staging approach (31.4 mm CL). Conversely, for N. norvegicus, the morphometric approach yielded higher measurements (between 27.2 and 30.4 mm CL) than the gonadal approach (26.0 mm CL). This discrepancy might stem from the intense fishing overexploitation conditions of N. norvergicus, leading to a physiological adaptation that enables earlier gonadal maturation at faster rates than morphometric adaptation. Further research is required to elucidate these discrepancies and the effect of overexploitation on physiological (i.e., mature gonads) and functional maturity (i.e., capacity to brood eggs at a larger size). Keywords: deep-sea lobsters; management; morphometry; maturity; Nephropidae Key Contribution: This research is the first comparative study on the morphological sexual maturity of Nephropidae species populations unexploited in the Colombian Caribbean and overexploited in the Mediterranean Sea. 1. Introduction Deep-sea crustaceans are important constituents of demersal megafauna, holding substantial potential for global fisheries [ 1 , 2 ]. The deep-sea clawed Nephropidae species, the Fishes 2024,9, 78. https://doi.org/10.3390/fishes9030078 https://www.mdpi.com/journal/fishes Fishes 2024,9, 78 2 of 16 Caribbean lobster Metanephrops binghami and the Norway lobster Nephrops norvegicus, are of high commercial interest [ 3 ]. Nephrops norvegicus inhabits the Mediterranean Sea and the Atlantic Ocean [ 3 ] and faces significant overexploitation, exceeding three times the maximum sustainable yield in the northwestern (NW) Mediterranean [ 4 ] (STECF 2022). Differently, M. binghami in the Colombian Caribbean Sea still remains, to date, unexploited [5]. Morphologically, both species are relatively small compared to other Nephropids such as Homarus spp. The mean cephalothorax length (CL) of M. binghami is approximately 34 mm [ 5 ], while that of N. norvegicus is around 30 mm [ 6 ]. Both lobsters show a very similar ecological niche and inhabit areas of soft sediments within self-made burrows, around which strong territorial behavior is associated [ 5 , 7 ]. Life trait similarities make M. binghami a valuable reference species to understand the effects of fishery management on exploited N. norvegicus stocks. The species establishes an unexploited baseline scenario for N. norvegicus stock recovery, given that the unexploited baseline was lost in Europe decades ago. For effective fisheries management, size at sexual maturity is an essential indicator for protecting immature individuals from exploitation while ensuring sustainable harvesting that aligns with the reproductive capacity of populations [ 8 , 9 ]. M. binghami has been poorly studied in the Colombian Caribbean Sea, while N. norvegicus has traditionally been an object of fishery studies relating size and reproductive cycle, especially in the Mediterranean Sea. The estimation of its average CL at sexual maturity has been made through analyses of the different stages of gonadal maturity and associations with size classes [ 10 – 12 ]. However, the estimation of size at sexual maturity based on gonadal status can be biased due to possible visual errors in assigning maturity stages. In crustaceans, there is difficulty in differentiating juveniles from adults by size structure due to the natural process of molting to shed their exoskeleton in order to grow larger [13,14]. Other methods, such as morphometric analyses, could describe allometric growth changes linked to maturity aspects, being less affected by temporal and demographic fluctuations [ 15 ]. The change in growth at the beginning of sexual reproduction in crustaceans can be identified by analyzing morphometric relationships with the aim of differentiating juveniles and adults, and thus size at sexual maturity [ 16 ]. Consequently, it is expected that patterns of morphometric variation indicate differences in growth, as the shape of the body is related to structural changes in the ontogeny of organisms; this is very important for implementing efficient fishery management strategies [8]. In Nephrops norvegicus, size at sexual maturity onset in variable fishery pressure conditions can be attributed to reduced somatic growth, as energy is being used for the construction of gonads at smaller sizes [ 12 , 17 – 20 ]. In crustaceans, this process produces body changes that can be detected by discontinuities of growth at the onset of sexual maturity [ 18 , 19 , 21 – 23 ]. As a result, such discontinuities allow for analyzing morphometric relationships to differentiate juveniles from adults, and therefore to determine the size at sexual maturity [ 16 ]. In unexploited habitats, the size at maturity of N. norvegicus is unknown because unexploited areas in the Atlantic and Mediterranean are absent. In highly exploited fisheries, a decline in the onset of maturity is expected due to the selective removal of larger and more mature individuals from the populations [ 24 ]. This can lead to a shift in these populations toward smaller and younger individuals, which can result in a decline in the average size at sexual maturity. N. norvegicus, which has been overexploited for decades in NW Mediterranean fisheries, has had a decline in the size at maturity of females from around 30 mm CL to around 25.3 mm CL in the last 25 years [ 20 ]. Similarly, in the Irish Sea, a decline in female size at onset of maturity from 23.6 to 20.6 mm in two decades has been reported for N. norvegicus [25]. Here, the demographic analysis of the ecologically equivalent and unexploited Caribbean M. binghami has strategic value for European fishery management. The morphometric approach has been successfully used to establish a morphometric breakpoint for M. binghami [ 26 ] and M. rubellus, the latter in a partially exploited fishery in the Atlantic Sea off Sao Paulo, Brazil [ 19 ]. This study aimed to compare the effectiveness of the morphometric Fishes 2024,9, 78 3 of 16 approach with the gonadal macroscopic approach to estimate size at sexual maturity for females of unexploited M. binghami and overexploited N. norvegicus. 2. Materials and Methods 2.1. Data Collection for M. binghami and N. norvegicus Samples of M. binghami were collected from the Colombian Caribbean Sea, between Punta Gallinas and the Gulf of Urabá(Figure 1A), in August and December 2009, March and May 2010, and from August 2020 to May 2021. Considering that Pérez et al. [ 26 ] reported the reproductive season for M. binghami to take place in October, the sampling encompassed both the reproductive and non-reproductive seasons, which enabled individuals from the entire size range to be evaluated. Sampling was carried out onboard a commercial bottom trawler, with an opening of 11.6 m at the footrope and a cod-end mesh size of 44.5 mm from knot to knot. A total of 87 fishing trawls were performed in depths ranging from 200 to 550 m, with at least two hauls per 100 m depth stratum. Each haul lasted 30 min and was conducted at an average speed of 2.5 knots. Size at sexual maturity was obtained for 490 females through visual gonadal stage classification, and for 199 females through the morphometric approach. Fishes 2024, 9, x FOR PEER REVIEW 3 of 17 Here, the demographic analysis of the ecologically equivalent and unexploited Caribbean M. binghami has strategic value for European fishery management. The morphometric approach has been successfully used to establish a morphometric breakpoint for M. binghami [26] and M. rubellus, the latter in a partially exploited fishery in the Atlantic Sea off Sao Paulo, Brazil [19]. This study aimed to compare the effectiveness of the morphometric approach with the gonadal macroscopic approach to estimate size at sexual maturity for females of unexploited M. binghami and overexploited N. norvegicus. 2. Materials and Methods 2.1. Data Collection for M. binghami and N. norvegicus Samples of M. binghami were collected from the Colombian Caribbean Sea, between Punta Gallinas and the Gulf of Urabá (Figure 1A), in August and December 2009, March and May 2010, and from August 2020 to May 2021. Considering that Pérez et al. [26] reported the reproductive season for M. binghami to take place in October, the sampling encompassed both the reproductive and non-reproductive seasons, which enabled individuals from the entire size range to be evaluated. Sampling was carried out onboard a commercial bottom trawler, with an opening of 11.6 m at the footrope and a cod-end mesh size of 44.5 mm from knot to knot. A total of 87 fishing trawls were performed in depths ranging from 200 to 550 m, with at least two hauls per 100 m depth stratum. Each haul lasted 30 min and was conducted at an average speed of 2.5 knots. Size at sexual maturity was obtained for 490 females through visual gonadal stage classification, and for 199 females through the morphometric approach. Figure 1. Sampling stations for M. binghami ((A), the Colombian Caribbean Sea) and N. norvegicus ((B), the NW Mediterranean Sea). Blueand orange-colored dots are the trawl sampling events used to gather gonadal and morphometric data. Samples of N. norvegicus were collected from deep-sea surveys in the northwestern Mediterranean Sea (Balearic Sea) along the Catalan coast (Figure 1B). ICATMAR [27] fishing monitoring program observers collected samples from 2019 to 2022, three times per month, on board bottom trawlers equipped with bottom-trawl nets with a cod-end mesh size of 40 mm squared. Surveys were carried out in slope areas where intensive fishing pressure has been occurring for decades [27]. A total of 197 fishing trawls were performed at 91 and 540 m on the Ebro Delta shelf and between 537 and 373 m on the slope off Blanes (see Figure 1B). The hauls lasted about 1.5 h at an average speed of 2.2 knots. Size at sexual maturity obtained by macroscopic examination of the color of the Figure 1. Sampling stations for M. binghami ((A), the Colombian Caribbean Sea) and N. norvegicus ((B), the NW Mediterranean Sea). Blueand orange-colored dots are the trawl sampling events used to gather gonadal and morphometric data. Samples of N. norvegicus were collected from deep-sea surveys in the northwestern Mediterranean Sea (Balearic Sea) along the Catalan coast (Figure 1B). ICATMAR [ 27 ] fishing monitoring program observers collected samples from 2019 to 2022, three times per month, on board bottom trawlers equipped with bottom-trawl nets with a cod-end mesh size of 40 mm squared. Surveys were carried out in slope areas where intensive fishing pressure has been occurring for decades [ 27 ]. A total of 197 fishing trawls were performed at 91 and 540 m on the Ebro Delta shelf and between 537 and 373 m on the slope off Blanes (see Figure 1B). The hauls lasted about 1.5 h at an average speed of 2.2 knots. Size at sexual maturity obtained by macroscopic examination of the color of the ovaries, based on Rotllant et al.’s [ 28 ] histological examination, was calculated for a total of 3433 females. A total of 116 females covering all size ranges were randomly selected for morphometric analyses. Given that the selective extraction of crustaceans in fisheries exploitation may modify size at sexual maturity, we compared the effectiveness of two methods to detect this change. Fishes 2024,9, 78 4 of 16 2.2. Morphometric Analysis Approach For the morphometric approach to determine size at sexual maturity for females of M. binghami and N. norvegicus, all specimens were measured using seven body descriptors to the nearest 0.01 mm [ 29 – 31 ]: total length (TL); cephalothorax length (CL); first abdominal segment length (FSL); first abdominal segment width (FSW); first abdominal segment height (FSH); hepatic spine width (HSW); antennal spine width (ASW) (Figure 2). Fishes 2024, 9, x FOR PEER REVIEW 4 of 17 ovaries, based on Rotllant et al.’s [28] histological examination, was calculated for a total of 3433 females. A total of 116 females covering all size ranges were randomly selected for morphometric analyses. Given that the selective extraction of crustaceans in fisheries exploitation may modify size at sexual maturity, we compared the effectiveness of two methods to detect this change. 2.2. Morphometric Analysis Approach For the morphometric approach to determine size at sexual maturity for females of M. binghami and N. norvegicus, all specimens were measured using seven body descriptors to the nearest 0.01 mm [29–31]: total length (TL); cephalothorax length (CL); first abdominal segment length (FSL); first abdominal segment width (FSW); first abdominal segment height (FSH); hepatic spine width (HSW); antennal spine width (ASW) (Figure 2). Figure 2. Morphometric measures of a female of M. binghami: total length (TL); cephalothorax length (CL); first abdominal segment length (FSL); first abdominal segment width (FSW); first abdominal segment height (FSH); hepatic spine width (HSW); and antennal spine width (ASW). 2.3. Data Analysis The morphometric approach to distinguish juveniles and adults was conducted by means of a principal component analysis (PCA) with two allometric independent variables—TL, CL—and six dependent variables—CL, FSL, FSW, FSH, HSW, ASW—all transformed in a log base. The individuals were assigned to the juvenile and adult groups using a hierarchical cluster. Individuals from both groups were then assigned based on their weight on the two axes of the PCA [32]. Then, a discriminant analysis was performed to assign individuals to the juvenile or adult classes on the basis of the X and Y allometric variables. Size at 50% maturity (L50%) was estimated using a logistic regression, meaning Figure 2. Morphometric measures of a female of M. binghami: total length (TL); cephalothorax length (CL); first abdominal segment length (FSL); first abdominal segment width (FSW); first abdominal segment height (FSH); hepatic spine width (HSW); and antennal spine width (ASW). 2.3. Data Analysis The morphometric approach to distinguish juveniles and adults was conducted by means of a principal component analysis (PCA) with two allometric independent variables—TL , CL—and six dependent variables—CL, FSL, FSW, FSH, HSW, ASW—all transformed in a log base. The individuals were assigned to the juvenile and adult groups using a hierarchical cluster. Individuals from both groups were then assigned based on their weight on the two axes of the PCA [ 32 ]. Then, a discriminant analysis was performed to assign individuals to the juvenile or adult classes on the basis of the X and Y allometric variables. Size at 50% maturity (L 50% ) was estimated using a logistic regression, meaning the length at which a randomly chosen specimen had a 50% chance of being mature [ 31 – 34 ]. In the regression analysis, X (independent explanatory variable) and Y (the dependent response variable) had two alternative statuses (binomial): juveniles: 0; adults: 1. To evaluate differences in linear relationships between the juveniles and adults, an analysis of co-variance was performed (ANCOVA) [35]. Fishes 2024,9, 78 5 of 16 2.4. Gonadal Maturity Analysis Approach Size at sexual maturity was estimated via the classification of female stages of gonadal maturity based on the macroscopic examination of gonadal coloring. Maturity was evaluated only in female individuals of both species, as the maturity of males cannot be ascertained by the macroscopic inspection of gonads [ 28 , 36 ]. For M. binghami, we used five macroscopic stages, which were validated through histological observation [ 26 ]: 1, white, immature; 2, opaque, in development; 3, yellow, maturing; 4, green, mature; and finally, 5, ovigerous, carrying eggs on its pleopods. For N. norvegicus, we also used five maturity stages supported by previous histological analyses [ 37 ]: 1, white, immature, slender and thin ovaries; 2, resting, cream-yellowish; 3, beginning of maturation, small, light green; 4, big, thick, light green; and finally, 5, dark green, with advanced maturations in pre-spawning or spawning phases, also referred to as berried females. The estimation of size at 50% maturity was carried out by equating the criteria defining maturity stages for both species. We defined mature females of M. binghami as those within stages 3 to 5, excluding stage 1 representing immature juvenile individuals and stage 2, representing individuals not yet mature, but in development. For N. norvegicus, mature individuals were defined from stage 2 to 5, with stage 1 representing immature juvenile individuals and those in development but not yet mature. The gonadal size at sexual maturity (L 50% , CL and TL) was estimated using a logistic regression of the Bayesian Generalized Linear Model (GLM) (R package). We calculated the parameters aand bof the logistic function [ 16 ], where P(L) is the mature female proportion. The size at 50% maturity was obtained by L50% = (−a/b) [11]. P(L)=1 1+exp(a+bL)(1) 3. Results The total length (TL) of females of M. binghami ranged from 63.80 to 160.18 mm (122.87 ± standard deviation (SD) 22.97 mm) and the cephalothorax length (CL) ranged from 18.42 to 46.05 mm (35.25 ± 6.63 mm). Nephrops norvegicus females showed TL between 75.70 and 140.50 mm (103.46 ±15.92 mm), and CL ranging from 22.26 to 44.36 mm (31.23 ± 5.13 mm). The morphometric relationships of M. binghami and N. norvegicus for both juveniles and adults were highly correlated between TL vs. CL, FSL, FSW, FSH, HSW, and ASW (Tables 1and 2). The ANCOVA showed statistically significant differences between parameter a(intercept) of females for both species in all linear relationships, as well as in parameter b(slope) between TL vs. FSW and FSH, and CL vs. TL, FSW, FSH, and HSW for M. binghami (Figure 3; Table 1). In contrast, there was no significant difference in parameter bfor N. norvegicus (Figure 3; Table 2) or M. binghami between TL vs. CL, FSL, HSW and ASW, or CL vs. FSL and ASW (Figure 3; Table 1). Juveniles were distinguished from adults for M. binghami and N. norvegicus (Figures 3and 4; Tables 1and 2) through morphometric relationships using discriminant functions. The size at sexual maturity of M. binghami, as estimated by the morphometric relationships, varied between 110.49 and 118.56 mm TL 50% (r 2 = 0.85–0.96), and 28.60 and 33.89 mm CL 50% (r 2 = 0.95–1.00) (Table 3). In contrast, the size at sexual maturity of N. norvegicus estimated by morphometric relationships varied between 92.85 and 100.65 mm TL 50% (r2= 0.87–1.00), and 27.20 and 30.40 mm CL50% (r2= 0.869–0.98) (Table 3). The sexual maturity of females of M. binghami (N = 490; Figure 5) obtained by gonadal visual classification showed a majority of them in a mature condition, with 71.0% mature and 29.0% immature. The size at sexual maturity (TL 50% ) of females was 108.98 mm TL (95% CI = 106.10–111.60) and 31.40 mm CL (95% CI = 30.60–32.20) (Figure 5). The logistic model parameters for TL 50% were specified as a= − 15.06 and b= 0.14, and for CL 50% as a=−15.57 and b= 0.50; r2= 0.75 in both cases. Fishes 2024,9, 78 6 of 16 Table 1. Parameters of morphometric relationships in females of M. binghami: total length (TL), cephalothorax length (CL), first abdominal segment length (FSL), first abdominal segment width (FSW), first abdominal segment height (FSH), hepatic spine width (HSW), and antennal spine width (ASW). N: number of specimens; r 2 : determination coefficient. The numbers marked in bold denote significant differences from intercept and slope of morphometric relationships. Relationship Characteristic NN (%) Intercept (a) Slope (b)r2p(ANCOVA) Intercept Slope TL vs. CL Juveniles 91 37.92 3.258 0.244 0.93 0.000 0.940 Adults 149 62.08 2.062 0.271 0.83 TL vs. FSL Juveniles 72 36.18 0.263 0.017 0.82 0.000 0.148 Adults 127 63.82 0.567 0.015 0.40 TL vs. FSW Juveniles 87 36.25 0.506 0.136 0.91 0.000 0.034 Adults 153 63.75 1.177 0.142 0.76 TL vs. FSH Juveniles 83 34.58 0.126 0.112 0.81 0.000 0.000 Adults 157 65.42 1.197 0.111 0.80 TL vs. HSW Juveniles 88 36.67 0.918 0.139 0.82 0.000 0.100 Adults 152 63.33 0.742 0.154 0.65 TL vs. ASW Juveniles 101 42.08 1.029 0.140 0.89 0.000 0.975 Adults 139 57.92 0.824 0.149 0.77 CL vs. TL Juveniles 91 37.92 4.926 3.406 0.93 0.000 0.038 Adults 149 62.08 14.061 3.125 0.83 CL vs. FSL Juveniles 34 17.00 0.361 0.054 0.75 0.000 0.367 Adults 166 83.00 0.501 0.053 0.65 CL vs. FSW Juveniles 68 27.87 −0.252 0.515 0.95 0.000 0.032 Adults 176 72.13 1.198 0.494 0.73 CL vs. FSH Juveniles 90 36.89 −0.932 0.445 0.93 0.000 0.000 Adults 154 63.11 2.086 0.366 0.69 CL vs. HSW Juveniles 108 44.44 −0.337 0.553 0.75 0.000 0.024 Adults 135 55.56 0.190 0.550 0.83 CL vs. ASW Juveniles 92 37.86 −0.184 0.548 0.93 0.000 0.097 Adults 151 62.14 0.750 0.521 0.85 Table 2. Parameters of morphometric relationships in females of N. norvegicus: total length (TL), cephalothorax length (CL), first abdominal segment length (FSL), first abdominal segment width (FSW), first abdominal segment height (FSH), hepatic spine width (HSW), and antennal spine width (ASW). N: number of specimens; r 2 : determination coefficient. The numbers marked in bold denote significant differences from intercept and slope of morphometric relationships. Relationship Characteristic NN (%) Intercept (a) Slope (b)r2p(ANCOVA) Intercept Slope TL vs. CL Juveniles 38 32.48 1.972 0.271 0.86 0.000 0.965 Adults 79 67.52 2.187 0.277 0.91 TL vs. FSL Juveniles 52 44.44 0.268 0.064 0.41 0.000 0.119 Adults 65 55.56 0.900 0.059 0.72 TL vs. FSW Juveniles 41 35.04 −1.341 0.161 0.84 0.000 0.702 Adults 76 64.96 −1.529 0.166 0.94 TL vs. FSH Juveniles 46 39.32 −0.729 0.141 0.63 0.000 0.527 Adults 71 60.68 −3.797 0.177 0.81 TL vs. HSW Juveniles 55 47.01 1.968 0.110 0.61 0.000 0.210 Adults 62 52.99 3.182 0.108 0.81 Fishes 2024,9, 78 7 of 16 Table 2. Cont. Relationship Characteristic NN (%) Intercept (a) Slope (b)r2p(ANCOVA) Intercept Slope TL vs. ASW Juveniles 34 29.06 0.680 0.043 0.22 0.008 0.598 Adults 83 70.94 1.104 0.049 0.38 CL vs. TL Juveniles 38 32.48 7.194 3.111 0.86 0.000 0.382 Adults 79 67.52 2.455 3.294 0.91 CL vs. FSL Juveniles 38 32.48 0.449 0.211 0.16 0.000 0.157 Adults 79 67.52 0.272 0.218 0.71 CL vs. FSW Juveniles 38 32.48 −0.700 0.521 0.93 0.000 0.719 Adults 79 67.52 −1.689 0.563 0.89 CL vs. FSH Juveniles 51 43.59 0.605 0.424 0.76 0.000 0.330 Adults 66 56.41 −2.043 0.548 0.75 CL vs. HSW Juveniles 38 32.48 −0.216 0.460 0.65 0.000 0.612 Adults 79 67.52 0.215 0.449 0.77 CL vs. ASW Juveniles 36 30.77 0.688 0.147 0.31 0.009 0.051 Adults 81 69.23 0.934 0.171 0.40 Table 3. Sizes at sexual maturity of M. binghami and N. norvegicus estimated by morphometric relationships using the discriminant functions method. C.I.: lower and upper confidence (95%); r2: determination coefficient. Species Relationship a b L50% C.I. L50% r2 M. binghami TL vs. CL −33.812 0.298 113.54 111.40 to 115.80 0.89 TL vs. FSL −80.267 0.674 118.56 117.00 to 120.00 0.96 TL vs. FSW −33.103 0.297 112.05 109.70 to 114.00 0.89 TL vs. FSH −49.059 0.447 110.49 108.70 to 112.40 0.93 TL vs. HSW −25.682 0.229 112.33 110.00 to 114.40 0.85 TL vs. ASW −42.749 0.367 117.30 115.00 to 119.20 0.92 CL vs. TL −291.793 9.190 31.75 31.70 to 31.80 0.99 CL vs. FSL −3599.811 125.883 28.60 28.58 to 28.60 1.00 CL vs. FSW −67.876 2.305 29.45 29.40 to 29.45 0.95 CL vs. FSH −259.571 8.247 31.47 31.45 to 31.50 0.99 CL vs. HSW −103.206 3.046 33.89 33.89 to 33.90 0.97 CL vs. ASW −5405.663 170.208 31.76 31.75 to 31.80 1.00 N. norvegicus TL vs. CL −1850.197 19.523 94.77 94.80 to 94.80 1.00 TL vs. FSL −46.534 0.502 92.85 90.60 to 95.00 0.90 TL vs. FSW −106.388 1.088 97.82 97.80 to 97.80 0.97 TL vs. FSH −2297.428 23.819 96.45 96.50 to 96.50 1.00 TL vs. HSW −58.452 0.589 98.84 96.60 to 100.80 0.93 TL vs. ASW −37.089 0.369 100.65 98.20 to 103.10 0.87 CL vs. TL −83.222 2.893 28.77 28.80 to 28.80 0.95 CL vs. FSL −456.153 16.772 27.20 27.20 to 27.20 0.98 CL vs. FSW −162.028 5.541 29.24 29.20 to 29.20 0.97 CL vs. FSH −55.302 1.859 29.67 29.10 to 30.30 0.93 CL vs. HSW −42.464 1.431 29.44 28.70 to 30.20 0.90 CL vs. ASW −36.346 1.190 30.40 29.60 to 31.10 0.86 The sexual maturity obtained by gonadal visual classification for N. norvegicus females (N = 3433; Figure 5) indicated a nearly equal distribution, with 50.4% classified as mature and 49.6% as immature. The size at sexual maturity (TL 50% ) of females was 87.60 mm TL (95% CI = 87.00–88.10) and 26.03 mm CL (95% CI = 25.80–26.20) (Figure 5). The logistic model parameters for TL 50% were specified as a= − 19.66 and b= 0.22, and for CL 50% as a=−17.81 and b= 0.69; r2= 0.60 in both cases (Figure 5). Fishes 2024,9, 78 8 of 16 Fishes 2024, 9, x FOR PEER REVIEW 6 of 17 Figure 3. Morphometric relationships using discriminant functions for juvenile and adult females of M. binghami. (A): TL vs. CL; (B): TL vs. FSL; (C): TL vs. FSW; (D): TL vs. FSH; (E):TL vs. HSW; (F): TL vs. ASW; (G): CL vs. TL; (H): CL vs. FSL; (I): CL vs. FSW; (J): CL vs. FSH; (K): CL vs. HSW; (L): CL vs. ASW. Figure 3. Morphometric relationships using discriminant functions for juvenile and adult females of M. binghami. (A): TL vs. CL; (B): TL vs. FSL; (C): TL vs. FSW; (D): TL vs. FSH; (E): TL vs. HSW; (F): TL vs. ASW; (G): CL vs. TL; (H): CL vs. FSL; (I): CL vs. FSW; (J): CL vs. FSH; (K): CL vs. HSW; (L): CL vs. ASW. Fishes 2024,9, 78 9 of 16 Fishes 2024, 9, x FOR PEER REVIEW 7 of 17 Figure 4. Morphometric relationships using discriminant functions for juvenile and adult females of N. norvegicus. (A): TL vs. CL; (B): TL vs. FSL; (C): TL vs. FSW; (D): TL vs. FSH; (E):TL vs. HSW; (F): TL vs. ASW; (G): CL vs. TL; (H): CL vs. FSL; (I): CL vs. FSW; (J): CL vs. FSH; (K): CL vs. HSW; (L): CL vs. ASW. Figure 4. Morphometric relationships using discriminant functions for juvenile and adult females of N. norvegicus. (A): TL vs. CL; (B): TL vs. FSL; (C): TL vs. FSW; (D): TL vs. FSH; (E): TL vs. HSW; (F): TL vs. ASW; (G): CL vs. TL; (H): CL vs. FSL; (I): CL vs. FSW; (J): CL vs. FSH; (K): CL vs. HSW; (L): CL vs. ASW. Fishes 2024,9, 78 16 of 16 48. Di Salvatore, P.; Sacristán, H.J.; Florentín, O.; Varisco, M.; Lovrich, G.A. Female reproductive output and potential recruitment of three fished southern king crab stocks from the Southern Atlantic Ocean. ICES J. Mar. Sci. 2021,78, 2628–2642. [CrossRef] 49. 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