Effect of gillnet selectivity on elasmobranchs off the northwestern coast of Mexico

Ocean and Coastal Management 172 (2019) 105–116

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Ocean and Coastal Management journal homepage: www.elsevier.com/locate/ocecoaman

Effect of gillnet selectivity on elasmobranchs off the northwestern coast of Mexico

T

Sergio Ramírez-Amaroa,b, Felipe Galván-Magañac,∗ a

Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015 Palma, Spain Laboratori de Genètica, Universitat de les Illes Balears, 07122 Palma, Spain c Instituto Politécnico Nacional (IPN), Centro Interdisciplinario de Ciencias Marinas, Av. IPN s/n, Colonia Playa Palo de Santa Rita, Apdo. Postal 592, C.P. 23096, La Paz, Baja California Sur, Mexico b

ARTICLE INFO

ABSTRACT

Keywords: Artisanal fishery Gillnet Management Northwestern Mexico Selectivity

The regulation of mesh size is important for the effective and sustainable management of fisheries using gillnets, which are the main fishing gear used in artisanal elasmobranch fisheries throughout northwestern Mexico. Gillnet selectivity studies focusing on elasmobranchs have generally evaluated the impact on target species, and information on bycatches remains scarce. This study assessed the impact of gillnet selectivity on both target elasmobranch species and bycatches, by varying the mesh size of gillnets. Sampling was performed from 2009 to 2015 in five artisanal fishing grounds located along the northwestern coast of Mexico. The species composition and ecological parameters of the elasmobranch communities that were caught, as well as the size structure and estimated selectivity models for the main species caught, were compared between four mesh sizes: 10.16, 15.24, 20.32 and 25.4 cm (stretched opening). Overall, 32 elasmobranch species were caught, nine of which were common to all mesh sizes. Our results indicate that the species composition of the catch varied with mesh size. While the small-sized sharks Mustelus californicus and M. henlei were the main species caught by gillnets with the smaller mesh sizes, the guitarfish Pseudobatos productus and Zapteryx exasperata, and the Pacific angel shark Squatina californica were the main species caught gillnets with the largest mesh sizes. Gillnet selectivity was estimated for these latter four species as well as for the horn shark Heterodontus francisci. Optimum length for these species varied widely, increasing proportionally to mesh size. These findings emphasize the difficulty of determining an optimal minimum mesh size for multi-species fishery in this area. Finally, recommendations for future directions according to the species' vulnerability to fishing are discussed, focusing on the development of effective strategies to initiate or strengthen the recovery of elasmobranchs of the northwestern coast of Mexico.

1. Introduction

2002; Humber et al., 2017). The rapid expansion of elasmobranch fishery over the past two decades has greatly increased fishing pressure on elasmobranch populations, which constitute a high percentage of the total world catch (Selgrath et al., 2018). In addition, elasmobranchs caught as bycatch represent approximately half of the reported elasmobranch landing according to worldwide official statistics, which makes it difficult to accurately assess the impact of fishing on elasmobranch populations (Bonfil, 2002). The North West of Mexico is a region characterized by high productivity and diversity of marine resources, which are influenced by the cold California current that flows southward and generates costal upwelling along this region (Young, 2001; Zaytsev et al., 2003). In this part of Mexico, artisanal fisheries are of primary economic and cultural importance – with approximately 250 fishing communities located along the coast – providing both food and employment to some of the

Artisanal fisheries or small-scale fisheries – with a relatively small capital and energy and with small fishing vessels making short fishing trips close to shore – comprise approximately 94% of the world's fishery and produce nearly half of the global fish supply for human consumption (McGoodwin, 1990; FAO, 2012; Chuenpagdee and Jentoft, 2015). Consequently, there is an increasing concern for improved management of the resources used by these artisanal fisheries, particularly over elasmobranchs species (sharks and rays), which are especially vulnerable to fishing exploitation due to their life-history traits (low fecundity, late maturity, and slow growth) (Stevens et al., 2000). Although in several countries there are a few industrial fisheries for elasmobranch, most of the landings are actually produced by artisanal fisheries all over the world, especially in developing countries (Bonfil, ∗

Corresponding author. E-mail address: [email protected] (F. Galván-Magaña).

https://doi.org/10.1016/j.ocecoaman.2019.02.001 Received 6 November 2018; Received in revised form 21 January 2019; Accepted 7 February 2019 0964-5691/ © 2019 Elsevier Ltd. All rights reserved.

Ocean and Coastal Management 172 (2019) 105–116

S. Ramírez-Amaro and F. Galván-Magaña

poorest sectors of the Mexican society (McGoodwin, 1980; RamírezAmaro et al., 2013; Finkbeiner and Basurto, 2015). Small-scale fisheries in the North West of Mexico use small fishing vessels (5–10 m long outboard-powered open boats) with a crew typically consisting of three or less than three people. These vessels make short (1–2 days) fishing trips using various fishing gears (bottom longlines, handlines, drift gillnets, or bottom-set gillnets; Bizzarro et al., 2009a; Smith et al., 2009; Cartamil et al., 2011; Ramírez-Amaro et al., 2013). Most elasmobranch landings in the North West of Mexico are performed by artisanal fisheries using gillnets as the main fishing gear (Smith et al., 2009; Cartamil et al., 2011; Ramírez-Amaro et al., 2013). These nets are used on the continental shelf (in waters < 100 m depth); they are made of monofilament, are 100–1500 m in length and up to 6 m in height, and with stretched opening of nominal mesh sizes ranging from 6 to 33 cm (Cartamil et al., 2011; Ramírez-Amaro et al., 2013). This type of gillnets is considered the most effective method for catching a great diversity of elasmobranchs. In the North West of Mexico these gillnets are used by artisanal fisheries for catching small coastal sharks (the most frequently caught genera are Galeorhinus, Mustelus, and Squatina) and rays (the most frequently caught genera are Myliobatis, Pseudobatos, and Zapterix) (Bizzarro et al., 2009a, 2009b, 2009c; Smith et al., 2009; Cartamil et al., 2011; Ramírez-Amaro et al., 2013). Knowing the selectivity parameters of fishing gear – defined as the proportion of fish available for a particular fishing gear – is crucial for interpreting catch data accurately, and for determining the size structure of fish populations; these selectivity parameters can even be incorporated into modern stock assessment models (Hamley, 1975; Sparre and Venema, 1992; Millar and Fryer, 1999; Maunder, 2002). The gradual increase in selectivity of fishing gear can be represented as a selectivity curve, which quantifies the probability that a fish species of a given length-class will be caught (Hovgård and Lassen, 2000). Passive fishing gears, such as gillnets, have size-related selective properties commonly described by bell-shaped curves (Millar and Holst, 1997; Millar and Fryer, 1999). Gillnet selectivity is mainly affect by mesh sizes – smaller fish pass through the meshes unharmed, while larger ones are not able to pass through them. Gillnet selection curves thus represent the retention probability of different mesh sizes for a given species (Clarke, 1960; Millar and Fryer, 1999). Despite their potential benefits for fisheries assessment and management, gillnet selectivity parameters are currently available only for a few shark species, such as the gummy shark Mustelus antarticus (Kirkwood and Walker, 1986), the finetooth shark Carcharhinus isodon, the Atlantic sharpnose shark Rhizoprionodon terraenovae, the bonnethead shark Sphyrna tiburo (Carlson and Cortés, 2003), the sandbar shark Carcharhinus plumbeus (McAuley et al., 2007), and the blacktip shark Carcharhinus limbatus (Baremore et al., 2012), and only for one ray species (the shovelnose guitarfish Pseudobatos productus) (MárquezFarias, 2005, 2011). All of the previous studies have focused on specific target species, and none of them has evaluated the impact of gillnets on the whole fish community that is exploited; a broader view is important for moving towards an ecosystem approach to fisheries (Browman and Stergiou, 2004). Little attention has been paid to understanding how elasmobranch catches are influenced by the size selectivity of gillnets, even when the high diversity of elasmobranchs caught by artisanal fisheries (over 60 species) has been well documented throughout the North West of Mexico (Bizzarro et al., 2009a, 2009b, 2009c; Smith et al., 2009; Cartamil et al., 2011; Ramírez-Amaro et al., 2013). The objective of this study was to increase the knowledge on gillnet selectivity, by evaluating gillnets of different mesh sizes, based on data from artisanal elasmobranch fishery in the North West of Mexico. To this end, the catch composition, diversity indices, and selectivity parameters for the most abundant elasmobranch species were calculated and compared according to mesh sizes.

Fig. 1. Location of the artisanal fishing grounds sampled from 2009 to 2015 along the northwestern coast of Mexico: 1, Queen; 2, Malarrimo; 3, Bahía Tortugas; 4, El Cardón; 5, Adolfo López Mateos. Table 1 Number of fishing trips made at the different artisanal fishing grounds sampled from 2009 to 2015 along the northwestern coast of Mexico. Fishing grounds

Mesh size (cm)

Queen Bahía Tortugas Malarrimo El Cardón Adolfo López Mateos

10.16

15.24

20.32

25.4

3 4 9 8 10

6 6 6 21 1

16 18 23 6 5

3 22 2 0 4

Table 2 Length at first maturity (L50) of the most frequently caught elasmobranch species. Specified measurement (SM): TL, total length; DW, disc width; F, females; M, males. Species

L50 (cm) F

M

SM

Source

Cephaloscyllium ventriosum Heterodontus francisci Mustelus californicus

78.38

74.24

TL

Bernal-Pérez (2017)

53.5 86.2

51.2 72.8

TL TL

Mustelus henlei Myliobatis californica Pseudobatos productus Squatina californica Sphyrna zygaena

65.8 98.1 111.8 99 200

63.5 59.1 95.1 99 193.7

TL DW TL TL TL

Zapteryx exasperata

70.05

67.42

TL

Castellanos-Vidal (2017) Pérez-Jiménez and SosaNishizaki (2010) Soto-López et al. (2018) Pelamatti (2015) Juaristi-Videgaray (2016) Villavicencio-Garayzar (1996) Nava-Nava and Márquez-Farías (2014) Cervantes-Guitiérrez (2018)

2. Material and methods 2.1. Data source Data were collected from 2009 to 2015 in five artisanal fishing grounds located on the northwestern coast of Mexico that were visited sporadically: Queen; Malarrimo, Bahía Tortugas, El Cardón and Adolfo López Mateos (Fig. 1). During field visits, the catch of each vessel that fished on that day was sampled, and fishermen were interviewed to 106

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Table 3 Selectivity curves for the normal (fixed-spread), normal (proportional spread), gamma, and lognormal selection models used for estimating gillnet selectivity for the species most frequently caught; mj is the mesh size for panel j and li is the midpoint of length-class i. Model

Selection Curve

Normal Fixed-spread (k, σ) Normal spread α mj (k1, k2)

[ 1]{f1 (j, 1)} + [ 2]{f2 (j , 1)}

exp

(L k·mj)2 2 2

k 2

·{L.mj} +

exp

(L k1·mj)2 2k2·m2j

k1 k2

·

Gamma spread α mj (α, k)

1

L 1)·k·mj

(

exp

1

L k·mj

Lognormal spread α mj (μ, σ) 1 exp L

µ 1 + log

( ) mj m1

2

log(L)

[ µ1

mj m1

log

2

L mj

1]· log 1 2

{

+

k2 2 2 1 2k2

L mj

· log(L)·log

·{m2j } L mj

· 1 k

+

·

2

L mj

( )} +

( ) mj m1

mj 1 log2 2 m1

1

µ1 2

· log

( )

mj 2 m1

2 2

2

Table 4 Elasmobranch species caught by different mesh sizes (A, 10.16 cm; B, 15.24 cm; C, 20.32 cm; D, 25.4 cm) from 2009 to 2015 along the northwestern coast of Mexico; n, number of specimens caught; %, percentage of appearance; CPUE, catch per unit effort. Species

Sharks Alopias pelagicus Alopias vulpinus Carcharhinus obscurus Carcharodon carcharias Cephaloscyllium ventriosum Galeorhinus galeus Heterodontus francisci Heterodontus mexicanus Hexanchus griseus Isurus oxyrinchus Mustelus californicus Mustelus henlei Mustelus lunulatus Prionace glauca Sphyrna lewini Sphyrna zygaena Squatina californica Triakis semifasciata Batoids Bathyraja spinosissima Gymnura marmorata Himantura pacifica Hypanus dipterurus Hypanus longus Myliobatis californica Myliobatis longirostris Narcine entemedor Platyrhinoidis triseriata Pseudobatos productus Raja velezi Rhinoptera steindachneri Urobatis concentricus Zapteryx exasperata

n

%

A

B

C

8

1 1

8 5 3 24 21 204 2

1 2 33 1

36 3 67

1 85 264 16 1

6 23 232

D 11 3 3 1 11 2 43

CPUE (Standard Error)

A

B

C

1.55

0.13 0.13

0.50 0.31 0.19 1.56 1.31 12.76 0.13

0.19 0.39 6.40 0.19

4.71 0.39 8.76 0.78 3.01 30.33

7

0.19 16.47 51.16 3.10 0.19

273

1.36 0.19

9 4

12

0.19 0.39

2

1

88

33

6

124

7 8 639

41 1 1

1 17

25

300

7 1 1 2 1 1 67

5 100 25 24 2 1

12 170 5 15 14 99 14

1 1 6

124 4 1 1 90

D 1.72 0.47 0.47 0.16 1.72 0.31 6.74

A

B

C

0.27 (0.27)

0.03 (0.03) 0.03 (0.03)

0.10 0.06 0.04 0.32 0.27 2.17 0.03

0.03 0.07 1.10 0.03

(0.03) (0.05) (0.38) (0.03)

0.90 (0.33) 0.08 (0.04) 1.68 (0.64)

(0.03) (0.95) (1.82) (0.53) (0.03)

0.15 (0.08) 0.58 (0.26) 5.83 (2.90)

1.10

0.03 2.87 8.63 0.53 0.03

42.79

0.23 (0.11) 0.03 (0.03)

0.56 0.25

1.88

0.03 (0.03) 0.07 (0.46)

0.13

0.16

11.50

2.06

1.16

16.21

0.44 0.50 39.96

0.19 3.29

3.27

18.76

6.43 0.16 0.16 0.00 19.44 0.63 0.16 0.16 14.11

0.19 0.19 12.98

0.75 10.63 0.31 0.94

0.65 13.07 3.27 3.15

0.88 6.19 0.88

0.26 0.13

0.16 0.16 0.94

0.13 2.50 0.63 0.63

(0.13) (0.79) (0.26) (0.26)

(0.05) (0.04) (0.02) (0.12) (0.13) (0.51) (0.03)

0.15 (0.12) 2.22 (0.62) 0.06 (0.03) 0.19 (0.15) 0.18 (0.06) 1.26 (0.42) 0.18 (0.09)

0.35 0.10 0.10 0.03 0.35 0.06 1.39

(0.24) (0.05) (0.07) (0.03) (0.21) (0.04) (0.49)

0.03 (0.03) 0.03 (0.03) 0.19 (0.11) 0.23 (0.19) 8.94 (1.80)

0.12 (0.05) 0.05 (0.03)

0.39 (0.39)

0.03 (0.02)

0.03 (0.03)

2.20 (0.95)

0.42 (0.22)

0.20 (0.12)

3.10 (1.10)

0.09 (0.05) 0.10 (0.06) 8.23 (1.25)

1.32 (0.76) 0.03 (0.03) 0.03 (0.03)

0.03 (0.03) 0.50 (0.25)

0.43 (0.19)

3.79 (0.87)

0.03 (0.03) 0.03 (0.03) 2.23 (1.22)

0.03 (0.03)

D

0.03 (0.03)

4.00 0.13 0.03 0.03 2.90

(1.44) (0.13) (0.03) (0.03) (1.93)

Table 5 Mean values (standard error) of community parameters for different mesh sizes. The number of fishing trips and the total number of elasmobranch species for each mesh size are also shown. Parameter

Number of fishing. trips Number of species Species richness (S) Shannon diversity index (H′) Species evenness (J′) Ecological dominance (D)

Mesh size (cm) 10.16

15.24

20.32

25.4

34 20 3.267 0.700 0.626 0.452

40 17 3.300 0.848 0.806 0.538

68 22 3.859 0.879 0.769 0.741

31 22 3.548 0.623 0.590 0.543

(0.34) (0.12) (0.06) (0.11)

107

(0.22) (0.06) (0.03) (0.08)

(0.18) (0.06) (0.02) (0.08)

(0.28) (0.09) (0.05) (0.09)

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2.2. Data analysis

Table 6 Pairwise test for multiple comparisons of mean rank sums (Dunn's test; Q) between four mesh sizes. Below diagonal, species evenness index; above diagonal, species richness index. Significance level *p < 0.05. Mesh size (cm)

10.16

10.16 15.24 20.32 25.4

2.07 2.28 0.52

15.24

20.32

25.4

0.65

2.45* 1.90

1.23 0.66 0.99

0.12 2.83*

3.24*

The following ecological parameters were calculated based on the number of specimens caught per fishing trip for each mesh size: species richness (S), Shannon diversity index (H′), evenness (J′) and ecological dominance (D). To test for differences between mesh sizes, these indices were compared using the Kruskal-Wallis rank sum test (K-W) and Dunn's test. The differences in catch composition (number of individuals of each species) between mesh sizes were also analyzed for the main species caught. To this end, a redundancy analysis was carried out using the CANOCO 4.5 package (Ter Braak and Smilauer, 2002). A distribution-free Monte Carlo permutation test was used to test for the significance of the mesh size effect. Sex-specific length-frequency distributions were constructed for species with 25 or more individuals caught and measured in each mesh size, and their size at maturity (L50; represents the length at which 50% of the fish have reached maturity) was added. The L50 data of the main species caught are shown in Table 2. For the main species caught (i.e. those species with 25 or more individuals caught and measured in at least three different mesh sizes), gillnet selectivity models were developed according to the method proposed by Millar and Holst (1997). Because male and female elasmobranchs had no evident morphological differences, catch data per length-class were not separated by sex for this analysis. The assumptions used in these models were: i) all mesh sizes have equal fishing power; ii) length at maximum selectivity is proportional to mesh size; iii) sampling is equal among all length classes; iv) catches by each mesh size are independent observations from a Poisson distribution; and v) the gillnet of selectivity curve has the shape of a gamma distribution. Four selectivity models were fitted to the length-class data for each mesh size using the “gillnetfunctions” package for R statistical software (Millar, 2003, 2010). The parameters of the selectivity models were estimated by fitting a general log-linear model:

log(ûij) = factor (j ) +

1•f1 (mi,

j) +

2•f2 (mi,

j),

where ûij is the expected catch of each species for length-class j and mesh size i, and f1 (mi, j) and f2 (mi, j) are the selectivity functions of mi and j (which are given in Table 3). Factor (j) indicates that a lengthclass is fitted as a factor in the model. The SELECT method was used allowing gillnet selectivity parameters to be estimated; this method uses maximum likelihood estimation to fit the selectivity models to the proportions of the total catch taken by each mesh size for each lengthclass. All gillnet selectivity models were applied to the main species caught. The deviance of the fitted models from the observed data was calculated as the sum of the squared residual values (model deviance).

Fig. 2. Redundancy analysis of the elasmobranch species most frequently caught in gillnets of different mesh sizes. Cv, Cephaloscyllium ventriosum; Hf, Heterodontus francisci; Mc, Mustelus californicus; Mh, Mustelus henlei; Mca, Myliobatis californica; Pp, Pseudobatos productus; Sz, Sphyrna zygaena; Sc, Squatina californica; Ze, Zapteryx exasperata. Triangles represent the centroids of each mesh size: 10.2, 15.2, 20.3 and 25.4 cm. The figure also shows the percentage of variance explained by benthic habitats (V), F-ratio of the regression model (F) and significance value (p).

document gear types, and the main characteristics of the gear used. For this study, data collection consisted in inspecting gillnets used by artisanal fleets. The fleets sampled were those that used at least a panel of one the following mesh sizes: 10.16 cm, 15.24 cm, 20.32 cm or 25.4 cm (stretched opening). The gillnets inspected were generally made of monofilament webbing, 300–450 m in length, and up to 6 m in depth; these gillnets were deployed on the continental shelf for 24 h before retrieval. On average, two gillnets with different mesh sizes were used per fishing vessel. Gillnets were randomly inspected in each vessel in each fishing ground. All elasmobranchs caught were identified, and the individuals of each species were counted, measured, and sex was recorded. Standard measurements used were total length (TL) and disc width (DW). The catch per unit effort (CPUE) was estimated for each species and each mesh size. CPUE was defined as the number of individuals per vessel per fishing trip. The number of fishing trips sampled in artisanal fishing grounds is shown in Table 1. Because fishing grounds are isolated, and because the fishermen in the study area are highly opportunistic changing gears and target species seasonally, the data collected could not be analyzed by fishing grounds, year, or season.

3. Results A total of 32 elasmobranch species (18 species of sharks and 14 species of batoids) were caught by all mesh sizes (Table 4). Twenty-two species were caught by the mesh size of 22.32 and 25.4 cm (one and five species were exclusive to these mesh sizes, respectively), followed by 20 and 17 species that were caught by mesh sizes of 10.16 cm (one species was exclusive to this mesh size) and 15.24 cm (two species were exclusive to this mesh size), respectively. Nine species were common to all mesh sizes. In all mesh sizes, the most important species in terms of relative abundance (contributing to more than 93% of the total abundance) were the shovelnose guitarfish (Pseudobatos productus, 25% total relative abundance), the brown smooth-hound (Mustelus henlei, 19%), the banded guitarfish (Zapteryx exasperata, 12%), the Pacific angel shark (Squatina californica, 11%), the horn shark (Heterodontus francisci, 10%), the bat ray (Myliobatis californica, 6.5%), the smooth hammerhead (Sphyrna zygaena, 3%) the gray smooth-hound (Mustelus californicus, 3%) and the swell shark (Cephaloscyllium ventriosum, 2%). In contrast, twenty-three elasmobranch species represented 7% of the 108

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Table 7 Mean size (MS, TL in cm) and standard deviation (SD) for the elasmobranch species least frequently caught by different each mesh sizes. Asterisks (*) indicates the species whose MS was measured as disc width. Species

Mesh size (cm) 10.16 MS

Sharks Alopias pelagicus Alopias vulpinus Carcharodon carcharias Carcharhinus obscurus Galeorhinus galeus Heterodontus mexicanus Hexanchus griseus Isurus oxyrinchus Mustelus lunulatus Prionace glauca Sphyrna lewini Triakis semifasciata Batoids Bathyraja spinosissima Gymnura marmorata* Himantura pacifica* Hypanus dipterurus* Hypanus longus* Myliobatis longirostris* Narcine entemedor Platyrhinoidis triseriata Raja velezi Rhinoptera steindachneri* Urobatis concentricus*

119.25 130.5 91.5 133 66.67 228

15.24 SD

21.80 58.56 – 9.95 –

44 69.5

13.44

79 92

– –

72

20.32

25.4

MS

SD

MS

SD

305

–

75 84.5

– 2.88

236.70 147.5 118.45 122.65 79.5

56.50 2.62 18.90 27.55 7.95

108.8

19.77

169.5 111.10

67.43 33.15

117.05 78 154.90

20.10 22.57 32.27

129.40

13.25

41.5

2.4

63.5

–

54.68 43

–

MS

SD

269.63 220.39 148 181.69 151.50

15.16 111.49 – 80.95 12.10

146.5

–

144.50

21.5

6.02 8.50

48.29

16.78

89

5.65

100

–

59.78 53.87

9.84 6.92

107 56

–

59.45 95.5 53

3.90 – –

Fig. 3. Length-frequency distributions of the elasmobranch species frequently caught by artisanal fisheries in the northwestern coast of Mexico for the different mesh sizes (A, 10.16 cm; B, 15.24 cm; C, 20.32 cm; D, 25.4 cm) that were used for developing gillnet selectivity models: Heterodontus francisci, Mustelus henlei, Pseudobatos productus, Squatina californica, and Zapteryx exasperata. Females are depicted in black and males in white. Dotted lines indicate size at maturity for females (F) and males (M).

total abundance (Table 4). With the exception of the leopard shark (Triakis semifasciata, 1.1% total relative abundance), the remaining 22 species contributed to less than 1% of total abundance; thus, given their

low abundance, these species can be considered as bycatch of gillnets. No significant differences were found between mesh sizes for the following parameters: species richness (K-W; H = 7.95, p = 0.06), 109

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Fig. 4. Length-frequency distributions of the elasmobranch species frequently caught by artisanal fisheries in the northwestern coast of Mexico in only one mesh size: Cephaloscyllium ventriosum, Mustelus californicus, and Sphyrna zygaena. Mesh sizes: A, 10.16 cm, and B, 15.24 cm. Females are depicted in black and males in white. Dotted lines indicate size at maturity for females (F) and males (M).

Fig. 5. Length-frequency distributions of Myliobatis californica caught by different mesh sizes (A, 10.16 cm; B, 15.24 cm; C, 20.32 cm; D, 25.4 cm). Females are depicted in black and males in white. The dotted lines indicate size at maturity for females (F) and males (M).

addition, length-frequency models were developed for the species that were frequently caught by only one mesh size (Cephaloscyllium ventriosum, M. californicus, and S. zygaena; Fig. 4). The analysis of length-frequency distributions showed a wide range of size classes and varied according to mesh size and species. The effect of mesh size on the proportion of immature specimens also varied according to species. Around 55% of H. francisci specimens, and 40% of M. henlei specimens, caught by 10.16 cm mesh size were immature (i.e., their TL was below length at first maturity). For the mesh size of the following length (15.24 cm), the highest percentages of immature specimens were S. californica, P. productus, and Z. exasperata, 90%, 85%, and 55%, respectively, while H. francisci and M. henlei showed the lowest percentages (20% and 2%, respectively) for this mesh size. The percentage of immature specimens caught was lower for the mesh sizes of 20.32 cm and 25.4 cm. Squatina californica had the highest percentage of immature specimens caught by these mesh sizes (80%), followed by P. productus (50%); for H. francisci, M. henlei, and Z. exasperata the percentage of immature specimens caught was virtually 0%. Similarly, negligible percentages of immature specimens were found in H. francisci and Z. exasperata for the largest mesh size (25.4 cm). In P. productus and S. californica, the percentage of immature specimens caught was substantially lower than that of the previous mesh size (20% and 45%, respectively). The decreasing pattern in the percentage of immature specimens caught with mesh size was not observed in M. californica, which showed an irregular pattern instead (Fig. 5). Gillnet selectivity models also varied according to species. The gillnet selectivity models developed, and the selection parameters

Shannon diversity (K-W; H = 6.01, p = 0.11) and ecological dominance (K-W; H = 7.78, p = 0.06; Table 5). However, there were significant differences in species evenness between mesh sizes (K-W; H = 14.79, p = 0.002; Table 6). The mean evenness value was indeed higher for 15.24 cm mesh size (J’ = 0.81), followed by the mesh sizes of 20.32 cm (J’ = 0.77), 10.16 cm (J’ = 0.63) and 25.4 cm (J’ = 0.59). According to the RDA analysis of the main species caught, there were significant differences in catch composition between mesh sizes (Fig. 2). The species most frequently caught by 10.16 cm mesh size were M. henlei (51% relative abundance; CPUE = 8.63), Mustelus californicus (16.5%; CPUE = 2.87) and M. californica (13%; CPUE = 2.23). For 15.24 cm mesh size the species most frequently caught was also M. henlei (30%; CPUE = 5.83), followed by P. productus (16%; CPUE = 3.10), Sphyrna zygaena (13%; CPUE = 2.50) and M. californica (11.5%; CPUE = 2.20). In the catches using 22.32 cm mesh size the most abundant species were P. productus (40%; CPUE = 8.23), Z. exasperata (19%; CPUE = 3.79), H. francisci (13%; CPUE = 2.17) and M. henlei (11%; CPUE = 2.22). Finally, S. californica (43%; CPUE = 8.94), P. productus (19%; CPUE = 4.00) and Z. exasperata (14%; CPUE = 2.90) were the species most frequently caught by 25.4 cm mesh size. Except for Alopias pelagicus, A. vulpinus, and Prionace glauca (whose specimens were larger than 2 m), the specimens caught by all four mesh sizes consisted of medium-sized species (< 2 m in TL) (Table 7). The length-frequency distributions, used for developing gillnet selectivity models, were constructed for H. francisci (for all mesh sizes), for M. henlei (for the three smaller mesh sizes), and for P. productus, S. californica, and Z. exasperata (for the three largest mesh sizes; Fig. 3). In 110

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Table 8 Gillnet selectivity parameters estimated for different models for the elasmobranchs species most frequently caught by artisanal fisheries in the northwestern coast of Mexico: Heterodontus francisci, Mustelus henlei, Pseudobatos productus, Squatina californica, and Zapteryx exasperata. The models in italics were selected as the ones producing the most favorable goodness of fit. Species

Model

Parameters

Model Deviance

Heterodontus francisci

Normal (fixed-spread) Normal Gamma Lognormal Normal (fixed-spread) Normal Gamma Lognormal Normal (fixed-spread) Normal Gamma Lognormal Normal (fixed-spread) Normal Gamma Lognormal Normal (fixed-spread) Normal Gamma Lognormal

k = 3.514, σ = 16.157 k1 = 3.809, k2 = 1.994 α = 10.669, k = 0.379 μ = 3.686, σ = 0.304 k = 5.796, σ = 32.809 k1 = 6.526, k2 = 4.629 α = 8.838, k = 0.796 μ = 4.406, σ = 0.373 k = 4.514, σ = 20.471 k1 = 4.628, k2 = 1.040 α = 19.688, k = 0.239 μ = 4.258, σ = 0.235 k = 2.937, σ = 20.265 k1 = 1.552, k2 = 3.018 α = 7.283, k = 0.413 μ = 3.869, σ = 0.310 k = 3.797, σ = 11.173 k1 = 3.937, k2 = 0.355 α = 47.228, k = 0.083 μ = 4.089, σ = 0.145

137.806 172.529 158.208 153.502 104.00 110.942 104.472 117.206 438.115 428.332 439.478 451.033 132.848 135.253 136.207 137.283 145.300 143.597 133.076 131.218

Mustelus henlei

Pseudobatos productus

Squatina californica

Zapteryx exasperata

populations (Benjamins et al., 2010). Although, in general, there were no significant differences in the ecological parameters estimated between the four mesh sizes analyzed, there were differences in the species composition of the catch. The small-sized sharks Mustelus henlei and M. californicus were the species most frequently caught by gillnets with the smaller mesh sizes (10.16 and 15.24 cm). Similar results have been reported for small coastal sharks such as M. antarticus (Kirkwood and Walker, 1986), Carcharhinus isodon, Rhizoprionodon terraenovae, Sphyrna tiburo (Carlson and Cortés, 2003), and C. limbatus (Baremore et al., 2012), which are caught mainly in gillnets with mesh sizes lower than 15 cm (stretched opening). Immature specimens of Sphyrna zygaena were also frequently caught by gillnets with a mesh size of 15.24 cm. While the head morphology of this shark (dorsoventrally flattened and laterally expanded) would prevent its passage through the smaller mesh sizes, this species is known to have a great turning ability (Kajiura et al., 2003). This behavior causes these sharks to become entangled in the nets by “rolling” into them, or by breaking meshes and gilling in these large holes (McAuley et al., 2007). The guitarfish Pseudobatos productus and Zapteryx exasperata, and the Pacific angel shark Squatina californica were the species most frequently caught by gillnets with the larger mesh sizes (20.32 and 25.4 cm). The fishing efficiency of these large mesh sizes may be related to the morphology of these species. Indeed, these three species are dorsoventrally flattened, and the fact that their heads are joined to large flexible pectoral fins makes it difficult for them to escape. MárquezFarias (2005) reported that specimens of S. productus are mostly retained in gillnets with smaller mesh sizes (12.7 and 15.24 cm). In this study, however, specimens of this species were mostly caught in gillnets with a mesh size of 20.32 cm, which may be related to body size. Average TL and length at first maturity (L50) are known to be lower in specimens from the Gulf of California than in specimens from the Pacific Coast; the specimens from these two areas are even considered to belong to two different populations (Sandoval-Castillo et al., 2004). Because specimens of Z. exasperata and S. californica inhabiting these areas are also recognized as belonging to two different populations (Castillo-Páez et al., 2014; Ramírez-Amaro et al., 2017), similar differences in gillnet selectivity are to be expected. Based on the frequency distribution of lengths at first maturity of elasmobranchs commonly caught in gillnets, we show that maturity is reached at a wide range of lengths. For S. californica, the optimum

estimated for each species, are shown in Table 8 and Fig. 6. For H. francisci, the normal (fixed-spread) model had the lowest deviance value, and an optimum length (length at maximum selectivity) that was estimated at 35.7 cm TL for 10.16 cm mesh size; optimum length increased to 85.4 cm TL for 25.4 cm mesh size. For M. henlei, the normal (fixed-spread) model also had the lowest deviance value; the optimum lengths estimated ranged from 58.9 to 117.6 cm TL for the mesh sizes of 10.16 and 20.32 cm, respectively. For P. productus, the normal model had the lowest deviance value, and optimum length was estimated at 70.5 cm TL for 15.24 cm mesh size; optimum length increased by almost 23 cm for the largest mesh size (25.4 cm). For Z. exasperata and S. californica, different selectivity models (lognormal and normal) had the lowest deviance values; however, for the smallest mesh size (15.24 cm), the optimum lengths estimated were similar in both species (58.5 and 62.3 cm TL for Z. exasperata and S. californica, respectively). For the largest mesh size (25.4 cm), optimum lengths increased to 97.8 and 98.6 cm TL for Z. exasperata and S. californica respectively. 4. Discussion 4.1. Gear selectivity Based on fisheries data, this study assessed the impact of the selectivity of gillnets of various mesh sizes on elasmobranchs along the northwestern coast of Mexico, both at the community and population level. A large variety of elasmobranch species were caught in gillnets of all mesh sizes used in artisanal elasmobranch fisheries throughout the study area. Although the diversity of elasmobranch varied according to geographic area, the fishing grounds, grouped in this study for sampling, belong to the same marine province “Warm Temperate Northeast Pacific” (Spalding et al., 2007), so analyzing them as a single group could have a low impact for the interpretation of the results. Nine species of elasmobranchs constituted ninety percent of the total abundance; while the remaining 7% was integrated by 23 species, which were considered bycatch. A high richness of species in bycatches has been observed in gillnet fisheries worldwide, for example in Peru (Alfaro-Shigueto et al., 2010), Canada (Benjamins et al., 2010), and Madagascar (Humber et al., 2017). The actual amount of elasmobranch bycatch in fisheries is difficult to estimate because bycatch of elasmobranchs is rarely incorporated into national or international statistics, even though it is crucial for the proper assessment of elasmobranch 111

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Fig. 6. Gillnet selectivity curves (on the left) and residuals (on the right) estimated for the elasmobranchs species most frequently caught by artisanal fisheries in the northwestern coast of Mexico: Heterodontus francisci, Mustelus henlei, Pseudobatos productus, Squatina californica, and Zapteryx exasperata. The colours of the selectivity curves correspond to the four mesh sizes: blue for 10.16 cm; black for 15.24 cm; red for 20.32 cm; and green for 25.4 cm. Filled and open circles represent positive and negative residuals, respectively. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.) 112

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Fig. 7. Percentage of elasmobranch species caught by different mesh sizes (A, 10.16 cm; B, 15.24 cm; C, 20.32 cm; D, 25.4 cm) in reference to the Red List categories of the International Union for Conservation of Nature (IUCN): EN, Endangered; VU, Vulnerable; NT, Near Threatened; LC, Least Concern; DD, Data Deficient. The categories shown above the dotted line are considered threatened. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

difficult to properly protect the main elasmobranch species inhabiting the study area. In elasmobranchs, population growth rates are more sensitive to the survival of specimens of certain sizes or life stages (Cortés, 2002). It has been proposed that the management of small coastal species should focus mainly on protecting juveniles and adults rather than age-0 individuals (Cortés, 2002). The fishing areas where immature specimens are frequently caught could be considered as nursery areas. Indeed, the artisanal fishing grounds sampled in this study are associated with coastal lagoon systems, which have actually been considered as nursery areas for some elasmobranch species (Cartamil et al., 2011; Ramírez-Amaro et al., 2013). In Myliobatis californica, a frequently caught species, length-frequency distribution overlapped for all the different mesh sizes; because of this, the assumptions of gillnet selectivity models were not met. Similarly to other rays (mainly belonging to the families Myliobatidae, Mobulidae, and Dasyatidae), the morphology of M. californica, characterized by a flattened body with broad pectoral fins (about twice as wide as they are long; White and Naylor, 2016), may have affected the selectivity of gillnets. Likewise, the large-sized sharks (≥150 cm TL) Alopias pelagicus, A. vulpinus, Carcharhinus obscurus, Galeorhinus galeus, Prionace glauca, and Sphyrna lewini were caught by all mesh sizes. These large sharks probably became entangled in gillnets due to their rolling behavior, as discussed above. Because catches of M. californica and catches of the larger sharks were independent of mesh size, they can be considered incidental catches in artisanal fisheries. Taking into account the Red List categories of the International Union for Conservation of Nature (IUCN), which were applied to the elasmobranch species caught by each mesh size (Fig. 7; Table 9), the highest percentage (37%) of threatened species (i.e., those species belonging to the categories “Endangered” and “Vulnerable” was caught in gillnets with 15.24 cm mesh size, followed by the mesh sizes 20.32, 25.4, and 10.16 cm, which represents 27%, 23%, and 20% of threatened species, respectively. In total, eight species of sharks were listed as threatened species: one was as “Endangered” (S. lewini), and seven were “Vulnerable” (A. pelagicus, A. vulpinus, Carcharodon carcharias, C. obscurus, G. galeus, Isurus oxyrinchus, and S. zygaena). According to Furlong-Estrada et al. (2017), who assessed the vulnerability of sharks distributed in the same study area, three additional shark species, C. falciformis, H. francisci, and S. californica, should be also classified as vulnerable species. These species, with lower resilience than that of other shark species from the northwestern coast of Mexico (due to their long reproductive cycle, low fecundity, and great longevity), are considered to be especially vulnerable to fishing (Furlong-Estrada et al., 2017 and references therein). In contrast to the threatened species mentioned above, small coastal sharks such as M. henlei and M. californicus, have life-history traits that

Table 9 Summary information in the IUCN Red List categories for all elasmobranch species caught by artisanal fisheries in the northwestern coast of Mexico. EN, Endangered; VU, Vulnerable; NT, Near Threatened; LC, Least Concern; DD, Data Deficient, NE, Not Evaluated. Species

Category

Source

Sharks Alopias pelagicus Alopias vulpinus Carcharhinus obscurus Carcharodon carcharias Cephaloscyllium ventriosum Galeorhinus galeus Heterodontus francisci Heterodontus mexicanus Hexanchus griseus Isurus oxyrinchus Mustelus californicus Mustelus henlei Mustelus lunulatus Prionace glauca Sphyrna lewini Sphyrna zygaena Squatina californica Triakis semifasciata Batoids Bathyraja spinosissima Gymnura marmorata Himantura pacifica Hypanus dipterurus Hypanus longus Myliobatis californica Myliobatis longirostris Narcine entemedor

VU VU VU VU LC VU DD DD NT VU LC LC LC NT EN VU NT LC

Reardon et al. (2009) Goldman et al. (2009) Musick et al. (2009) Fergusson et al. (2009) Villavicencio-Garayzar et al. (2015) Walker et al. (2006) Carlisle (2015) Garayzar (2006) Cook and Compagno (2005) Cailliet et al. (2009) Perez-Jimenez et al. (2015) Perez-Jimenez et al. (2016) Perez-Jimenez et al. (2016) Stevens (2009) Baum et al. (2007) Casper et al. (2005) Cailliet et al. (2016) Carlisle et al. (2015)

LC LC NE DD DD LC NT DD

Provost et al. (2015) Bizzarro and Smith (2012)

Platyrhinoidis triseriata Pseudobatos productus Raja velezi Rhinoptera steindachneri Urobatis concentricus Zapteryx exasperata

LC NT DD NT DD DD

Smith et al. (2016) Smith (2016) van Hees et al. (2015) Smith and Bizzarro (2006a) Villavicencio Garayzar and Bizzarro (2009) Lawson et al. (2016) Farrugia et al. (2016) Valenti and Kyne (2009) Smith and Bizzarro (2006a,b) Bizzarro (2006) Bizzarro and Kyne (2015)

lengths estimated for all mesh sizes were shorter than lengths at first maturity. This implies greater fishing pressure on the immature population. A similar scenario was observed in S. zygaena, even though length at maximum selectivity was not estimated for this species. In contrast, for both H. francisci and M. henlei, optimum lengths were longer than the length at first maturity for almost all mesh sizes, implying greater fishing pressure on the mature population. In guitarfish, on the other hand, mesh size affected practically the whole population. The relationship between mesh size and length at maturity makes it 113

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make them less susceptible to fishing (e.g., early maturity, shorter generation time, and fast growth) (Castro, 2009; Pérez-Jiménez and Sosa-Nishizaki, 2010; Soto-López et al., 2018), which gives them greater resilience and recovery capacity in comparison with the shark species mentioned above (Au et al., 2015). These biological characteristics make it possible to exploit these shark species in a sustainable way, as has been proposed for M. antarticus (Walker, 1998). However, further studies (e.g., analysis of fishing mortality, population structure analysis, demographic analysis, and stock assessment) are needed, in order to achieve sustainable management of the species.

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Gymnura marmorata. The IUCN Red List of Threatened Species 2012: e.T14134429A14134464. https://doi.org/10.2305/IUCN.UK.2012-1. RLTS.T14134429A14134464.en. Bizzarro, J.J., Smith, W.D., Castillo-Geniz, J.L., Ocampo-Torres, A., Marquez-Farias, J.F., Hueter, R.E., 2009b. The seasonal importance of small coastal sharks and rays in the artisanal elasmobranch fishery in Sinaloa, México. Pan-Am. J. Aquat. Sci. 4, 513–531. Bizzarro, J.J., Smith, W.D., Hueter, R.E., Villavicencio-Garayzar, C.J., 2009c. Activities and catch composition of artisanal elasmobranch fishing sites on the eastern coast of Baja California Sur, Mexico. Bull. South Calif. Acad. Sci. 108, 137–151. https://doi. org/10.3160/0038-3872-108.3.137. Bizzarro, J.J., Smith, W.D., Marquez-Farias, J.F., Tyminski, J., Hueter, R.E., 2009a. Temporal variation in the artisanal elasmobranch fishery of Sonora, Mexico. Fish. Res. 97, 103–117. https://doi.org/10.1016/j.fishres.2009.01.009. Bonfil, R., 2002. 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4.2. Implications for management and conservation The Mexican elasmobranch fishery is multi-species and multi-gear, meaning that fishermen use different types of fishing gear to harvest elasmobranchs. Because of this, taking appropriate management and conservation measures is a difficult task for fishery managers. Various management measures have been implemented for Mexico's elasmobranch fishery. These measures include, stopping issuing shark fishing permits (Castillo-Geniz et al., 1998), developing a national action plan for the management and conservation of shark, rays and related species (CONAPESCA-INP, 2004), adopting a major piece of legislation that includes regulations that are specific to artisanal fisheries (NOM-029PESC-2006; DOF, 2007), and closing the shark and rays fishing season from May to July, to allow as many species as possible to reproduce (DOF, 2012). According to the results of the present study, our main conclusions and recommendations are as follows: i) A large variety of elasmobranch species were caught by all mesh sizes, and most of these species were bycatch, ii) mesh size affects both the species composition of the catch and the size at which the main species are caught in gillnets; iii) several factors can affect the selectivity of gillnets, including fish size, species composition, fish body shape, and fish behavior; iv) given the wide variety of life-history traits exhibited by the elasmobranchs that are commonly caught in gillnets, no single mesh size can optimize the yield of all the exploited species; v) the use of larger mesh sizes (> 25 cm) to catch S. californica would reduce fishing pressure on juvenile specimens, which would help the recovery of the population of this species; and vi) restricting the use of gillnets, or at least increasing their mesh size in breeding or nursery areas, such as coastal lagoons, could optimize output levels while protecting juvenile specimens, so that the lost specimens can be replaced. These management measures will initiate or strengthen the recovery of elasmobranchs, whose populations play an important role in marine ecosystems, off the northwestern coast of Mexico. These management measures will also help to develop true adaptive management in the area, making the artisanal fisheries compatible with the conservation of marine ecosystems. Acknowledgments The authors wish to thank all the students who participated in field data collection. They also greatly appreciated the patience, cooperation, and assistance of the artisanal fishermen operating at the studied fishing grounds who provided access to their landings and information about their fishing activities. This research was supported in part by the Consejo Nacional de Ciencia y Tecnologia (CONACYT) through an FPI scholarship to SRA and the project: “Ecología trófica de los elasmobraquios en Bahía Tortugas, Baja California Sur, Secretaría de Investigación y Posgrado [SIP] No. 20170563 and “Biología básica de las especies de tiburones y rayas de importancia comercial en la costa occidental de Baja California Sur”, CONACyT No. 253700. FGM thanks Instituto Politécnico Nacional for fellowships (Comisión para el Fomento de Actividades Académicas [COFAA] and Estímulo al Desempeño de los Investigadores [EDI]). Three anonymous reviewers and the Editor are also greatly acknowledged for their constructive comments in improving the quality of the manuscript. 114

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