BYCATCH OF THE ARTISANAL IN THE GULF OF (SONORA AND SINALOA)

Report prepared by Alejandro Balmori Ramírez (INAPESCA, CRIP-Guaymas) and Rufino Morales Azpeitia (CIBNOR-Unidad Guaymas), in collaboration with Everardo Miranda Mier and Jesús Guadalupe Padilla Serrato.

Guaymas, Sonora, México. June 2012

Summary

One of the most important fishing resources in Mexico is shrimp, this is due to its high economic and social value. Nonetheless, many non-target are captured incidentally during shrimp-fishing activities, and grouped as faunal companions or shrimp bycatch (SBC). Most of the SBC species have not been studied and the impact of this fishery upon them is yet unknown. This document presents the results of a study on the artisanal shrimp ’ bycatch within the bays of Guaymas, Bahía de Lobos, and El Tóbari, in the State of Sonora; and in Santa Maria La Reforma in the State of Sinaloa, during the 2011–2012 shrimp fishing season. The study collected shrimp and SBC samples, identified the organisms to the species level, and recorded biological sampling (biometrics). Logbook data and sampling information was captured in a database. We documented 854 fishing hauls for all of the bays. SBC analysis shows a total composition of 46 identified species belonging to different taxonomic groups such as , , gastropods, and elasmobranchs, and an additional 10 species identified to the level only. The most diverse group was that of bony fishes and the most dominant species was the swimming (Callinectes spp.). The amount of SBC species varied spatially ( system). During the shrimping activity, a high percentage (20-30%) of negative fishing hauls (i.e., without any SBC captures) was recorded, indicating that the artisanal shrimp fishery does not generate any bycatch in a third of all fishing hauls. The SBC shrimp ratio average for all bays was 1:0.5, and ranged from 1:0.28 to 1:10.5 — a lower proportion than the reported ratios of 1:8 (Amezcua et al. 2006) and 1:22 (Suenaga 2010). SBC species are mostly discarded (75%), with only some species being retained (25%), and these are used for their commercial value and for consumption (e.g., sand bass ( maculatofasciatus), sierra (Scomberomorus sierra), seabass (Cynoscion spp.), mojarras (Eucinostomus spp.), and swimming (Callinectes spp.)). Regarding species under special protection, only one individual of Mycteroperca jordani was captured, a species classified as endangered according to the IUCN, although its frequency of occurrence is 0.003 per thousand fishing hauls. We concluded that the impacts of the artisanal shrimp fishery upon the SBC are low, due to the low amount of bycatch that is generated, the low ratio of the capture to SBC species, and the lack of presence of threatened or endangered species in the SBC. Finally, it is recommended to continue studying the SBC during other fishing seasons and to analyze the population dynamics of the dominant species to determine the health status of these populations, since they may be indicative of impacts.

INTRODUCTION

In Mexico, fishing is important because of its annual production volume of about 1.5 million metric tons and the number of people who depend on it directly or indirectly (SAGARPA 2007). However, when any resource is fished, the capture includes non-target species, commonly known as faunal bycatch (FBC). The shrimp bycatch (SBC) represents the species of flora and fauna that are not a target of this fishery, and is known throughout the world as "bycatch" or as "non-target" species (FAO 1997).

Global estimates of SBC range from 5 to 16 million metric tons, with shrimp fisheries generating the highest incidental catch volumes, with a ratio of shrimp to SBC of about 1:5 in temperate or subtropical waters and of 1:10 in tropical areas (FAO 1999). It is estimated that annually between 3 and 7.5 million metric tons of SBC are discarded in the world (Allsop 1977, Morgan and Chuenpagdee 2003, and Kelleher 2005). In particular, the offshore shrimp fishery, with larger vessels, contributes to the bycatch problem due to the fishing system used: the trawl net. Although bycatch is also captured by smaller boats (pangas) using other fishing gear such as cast nets, trawl nets (“change” nets), suripera nets, and gillnets (Amezcua et al. 2006; SEMARNAP, INAPESCA 2000).

Fishing activities are particularly striking in a marine environment, directly affecting almost all habitats except for the deep sea, where no fishing takes place. Even with the more restrictive management practices enforced today, fisheries can have deep impacts on the marine environment, ranging from overexploitation of species due to extraction, to incidental capture problems, habitat alteration, genetic changes in populations, and affecting the structure of food webs (Anonymous, 2000).

The problem of bycatch has gained importance in recent decades, and viable solutions have been sought, ever since the FAO Technical Conference on Fishery Products was held in Tokyo in 1973, and later the conference of the International Research Center for Development in held Bangkok in 1974 (Pérez-Mellado et al. 1982). Since then and until the present, there have been a series of international workshops in search for solutions.

Shrimp is one of the most important resources due to its high economic value, generating trade income for the country and supplying a source of employment. Some estimate it creates 37,000 jobs (SAGARPA, 2006). However, shrimp fishing is strongly criticized for its high SBC capture rates. In the Gulf of California, the SBC captured by fishing vessels comprises approximately 242 benthic-demersal species, as well as crustaceans, mollusks, and echinoderms, with fish being the dominant group (Nava- Romo 1994, López-Martínez et al. 2010, Madrid-Vera et al. 2010). Only a few of the SBC species have been studied (López-Martínez et al. 2007, Rábago Quiroz et al. 2008, González-Ochoa et al. 2009, Arzola-Sotelo 2010, Morales-Azpeitia et al. 2011).

Fishing vessels contribute between 60 and 70% of the total shrimp production, operating with two trawl nets with an average length of 95 feet (Heredia-Quevedo 2001). These nets are distinguishable by their

lack of selectivity, since they capture large volumes of fish, crustaceans, and mollusks (López-Martínez et al. 2000, 2007, Alverson et al. 1996; Pérez-Mellado 1998).

The artisanal Sonoran vessels that fish for shrimp in the riverside zone mainly employ entanglement nets, also known as “chinchorro de línea”; in the State of Sinaloa, fishermen employ a fishing gear known as the “suripera”, whish is a modified cast net. Many SBC species are captured during these fishing activities, but before this report, they had not been studied (Amezcua et al. 2006, Suenaga 2010). This study will determine the specific composition of organisms caught in the artisanal shrimp fishery within the main shrimping bays in the Gulf of California, particularly in the States of Sonora and Sinaloa.

Importance of the shrimp resource

Mexico has large areas of coastline, bays, and estuarine systems, all with great diversity of species. Among the most important groups found in the region are crustaceans, the group to which penaeid belong to (Leal-Gaxiola 1999). The shrimp fishery is one of the most important in the country, generating a large number of jobs. It is also one of the products that finds a high price in the international markets, generating high foreign exchange earnings for the country (Avila-Pardo 2001).

Currently, Mexico is among the world’s top ten shrimp producers (Gillett 2010). The Mexican shrimp production yield in the year 2000 was of around 70,144 metric tons (MT), with 52% corresponding to the Pacific ’s production, and the states of Sonora and Sinaloa its main producers (Herrera-Valdivia 2002). Usually, only two species of shrimp are exploited, the blue shrimp (Litopenaeus stylirostris) and the brown shrimp (Farfentepenaeus californiensis) (López-Martínez 2000).

The development of an artisanal fishery encourages the employment of large numbers of fishermen, who are organized into cooperatives, creating opportunities for economic development in their coastal communities; additionally, they produce food for human consumption, both locally and regionally. Currently, however, the economic return from this fishery is considered at the point of a full collapse (Cruz-Romero et al. 1996), due to lower catches and lower prices (Padilla-Serrato 2005).

Background

The shrimp resource is exploited by two fishing fleets, the first is composed of larger offshore vessels (ship) and the second, known as the or artisanal fleet, consists of smaller panga- boats. The bays in the states of Sonora and Sinaloa maintain constant contact with the sea, and due to their higher evaporation rates they have higher salinity conditions than the surrounding marine area. The dominant species of shrimp in Sonora is the blue shrimp, Litopenaeus stylirostris (Hernandez-Carballo and Macías 1996), with 90% of the catches, and therefore the coastal fisheries in the state are of great importance due to the higher market value of this species in the US market. This fishery is carried out during the species' different life stages and within different bodies of water: one taking place within protected bodies

(bays and ), in which artisanal-type fishing systems are used, and the other using larger offshore vessels (García-Bourbon et al. 1996).

The shrimp fishery inside protected waters dates back to pre-Hispanic times, and it is the oldest in the Mexico. The main states where this fishery is done are: Sinaloa, Sonora, Chiapas, Oaxaca, Nayarit, and Baja California Sur (Hernandez-Carballo and Macías 1996). The fishery inside the lagoon systems of Sonora is based in the southern part of the state, the most productive bays being: Guásimas, Lobos, Huatabampo, Yávaros, and Agiabampo. The artisanal shrimping season starts in late August and early September. This is known as the “bay shrimp fishing period,” and fishing can last between two and three weeks, until it reaches 70% of its total production, with the most common tail-sizes being small (70–90 mm) and medium (95–105 mm); subsequently, all small vessels move to the shore area (deeper area), in which larger organisms are captured (Herrera-Valdivia et al. 2002). Currently, this fishery has a management scheme with an established fishing ban period from the month of April to September, but the dates may vary according to the processes of mass spawning, growth, and the intensity of adult recruitment within the fishing areas (Aragon-Noriega 2000).

Artisanal or near-shore fishing is done on “pangas” (small boats about 7 m in length on average, with an outboard motor), right off the coastline at depths between 2 and 20 m. This is where most of the blue shrimp (L. stylirostris) is caught, using entanglement nets with mesh sizes ranging from 2 to 2 ½ inches. Suripera nets are used inside the bays, with mesh sizes between 1 ¼ and 1 ¾ inches, and are operated with the aid of a sail or motor working against the currents. Entanglement nets are also used, with a mesh size of 2 and 2 ¼ inches, as well as “atarraya” cast-nets. The efficiency and selectivity of the latter two fishing gears is very high (Anonymous 1995). This fishery is usually based on the capture of juvenile shrimp and is of enormous importance to fishermen in the months of August and September (Mendez- Tenorio 2001).

Blue shrimp biology These organisms are an important component of tropical marine and estuarine systems, where they are found inhabiting the shallow areas of estuaries and down to depths ranging to 1000 meters on the (Garcia and Le Reste 1987). Their life cycle depends on estuarine systems for their development and later they return to the open sea where they spend their adult and reproductive phases (Fig. 1). This indicates that they are exposed to changing environments that affect their abundance and the degree of this influence varies according to their development, thus their physiology is modified, developing a certain faculty for osmoregulation. This is because they migrate to different biotopes throughout their life cycle that are characterized by their salinity gradient (López-Martínez 2000). Environmental changes can affect the reproductive dynamics of stocks, inducing changes in their reproductive period (Leal-Gaxiola et al. 2001). Yields in the fishing season will depend on the effectiveness of the annual class, and this in turn reflects in recruitment success (Garcia and Le Reste 1981). The postlarval phase is essential for recruitment with larval rearing conditions reflecting upon the strength of the year’s class and these will in turn reflect upon catch volumes (Aragón-Noriega and Garcia-

Juarez 2002). Migration strategies and the effects of external factors on spawning success will help project the capture trends in the following fishing season. Factors such as wind, currents, and postlarval migration have an indirect influence on the success of a given year’s cohort, depending on the trajectories they take and the habitat in which they are placed. If the larvae are carried off to places with little or inadequate food sources, then spawning will fail; but under favorable environmental conditions it will succeed (Sinclair 1988, Bakun 1996). The blue shrimp (L. stylirostris) is a whose larval stage depends upon wetlands for breeding, spending up to two months of its life cycle inside them (Fig. 1). At an individual level these organisms are partial spawners, but at the population level they are massive spawners (Aragon-Noriega 2000, Lopez-Martinez 2000). This species is found from Punta Abreojos, Baja California Sur, Mexico, to Tumbes, , and it is not evenly represented along the coastline (Hendrickx 1995). L. stylirostris has a sex ratio of 1:1 (Rodriguez de la Cruz 1981, Rabago-Quiroz 2000). Its breeding season displays the same pattern as the spawning duration, but shrimp will mature first in Guaymas (March), then in Puerto Peñasco (April). In both regions, spawning reaches a maximum in June and July. The breeding season for blue shrimp in the Mexican Pacific coastline occurs from early March until September, with a maximum peak in May and June. The length at first maturity has been reported between 162 and 167 mm, at an age of 10 months (Rabago-Quiroz 2000). In its first larval stage, the nauplius uses its own yolk reserves. In the laboratory, protozoea are fed with phytoplankton and the mysis stage larvae are fed with and phytoplankton. Juveniles and adults in the wild are considered omnivorous or bottom feeders.

Figure 1. Life cycle of the Penaeid shrimp: a) eggs; b) nauplius; c) protozoea; d) mysis; e) postlarva; f) juvenile; g) adult; h) breeder (Modified from Benfiel 1999).

GENERAL OBJECTIVES

To determine the impact of the artisanal blue shrimp fishery on incidental catch in the states of Sonora and Sinaloa.

Specific objectives

• Determine the composition of the incidental catch • Describe the retained bycatch • Describe the discarded bycatch • Describe the globally threatened species found in the incidental catch of this fishery

MATERIAL AND METHODS

Study Area

The area of study comprised the following coastal : the bays of Guaymas, El Tobari, and Bahía de Lobos in the State of Sonora; and the bay of Santa Maria La Reforma in the State of Sinaloa. These bays are the most important in terms of the coastal shrimp fishery. The Gulf of California (GoC), or Sea of Cortez, is a marginal sea located in the Eastern Tropical Pacific . It is 1,400 km long, 200 km wide, and 3,600 meters deep; its waters wash upon the mainland states of Sonora, Sinaloa, and Nayarit, and also upon the states of Baja California and Baja California Sur on the Baja California Peninsula. The GoC is a great basin ocean, with oceanographic features that are the product of its submarine physiography and of the islands that are present in this region. The tides in the GoC are mainly caused by co-oscillation with the tides of the Pacific Ocean, meaning that sea level variations in the Gulf are mainly due to changes in sea level at the mouth of the Gulf, and not due to the gravitational pull of the sun and moon on the Gulf’s waters. Oceanographic conditions are different in the upper and central Gulf of California regions, because the islands act as ecological and physiographic barriers, leading to large planktonic blooms that are the basis of the food chain involving large numbers of fish and shellfish, and, therefore, many fisheries (Marinone and Lavin, 1997).

The GoC is divided into four regions: the Upper Gulf, the Northern region, the Southern region (which houses the study site), and the Mouth area. The GoC’s varying topography and bathymetry creates differences in the physical processes that control water circulation and its thermohaline structure (Thomson et al. 1969, Lavin et al. 1997). The Southern region is the largest area with a relevant bathymetric feature, the continental shelf on the peninsula’s side is almost nonexistent, but on the continental side ( of Sonora and Sinaloa) it averages 30 km.

Bay of Guaymas-Empalme

The Bay of Guaymas is a coastal body of water separated physiographically from the Gulf of California by a sandbar, communicating with the adjacent sea by means of a 1.2 km-wide mouth; its area measures 33.6 km2 and its average depth is 3 meters. It also has varied habitats, such as shallow waters, sandy and rocky beaches, islands, coastal dunes, vegetation, and algae beds. It is also site of breeding and rearing of shrimps, crabs, and various fish species, such as mullets, bass, and flounders. It is also a feeding and resting place for waterfowl. The El Rancho , the Empalme lagoon, and the Bay of Guaymas, are one integrated lagoon system, which herein will be generically called the Bay of Guaymas. It is located in the central portion of the eastern coast of the Gulf of California at 27o 55' N and 110o 53' W (Fig. 2).

Figure 2. Bays of Guaymas-Empalme and Guásimas, Sonora.

Bahía de Lobos

The Bahía de Lobos bay is located at the middle portion of the eastern coast of the Gulf of California, in the southern part of the state of Sonora. It is located between 27° 18' and 27° 26' N and 110° 27' and 110° 36' W. The water surface area of this lagoon is about 11,800 ha. Isla Lobos, a sand bar that gives this lagoon its shape, has a length of 17.5 km and an area of 1,950 ha. It has two permanent mouths: Boca de las Piedras, known as the Northern mouth (Boca Norte), with a width of 2.4 km; and the Southern Mouth (Boca Sur), which is 0.8 km wide. In the inner portion of the bay there are several deep

channels, large shallow areas, and mudflats, with plenty of marshes and intertidal channels (Arreola- Lizarraga 1995).

Figure 3. Bahía de Lobos, Sonora

El Tóbari Bay

This coastal lagoon is located between 26° 54' and 27° 10' N and 109° 50' and 110° 24' W. The island of Tóbari almost completely encloses this water body, communicating with the Burabampo estuary on its southeast portion. The system comprises several water bodies, including the Ensenada of La Batea (7.7 ha), the Chilico estuary (1.1 ha), Giamora (65.9 ha), La Liebre (23.4 ha), La Pitahaya (50.7 ha), Tóbari (6421.1 ha), the Ensenada El Gallo (29.9 ha), Punta Verde estuary (14.6 ha), El Conchalito (55.1 ha), El Tobarito (1038.1 ha), La Peninsula (111.8 ha), La Pitahaya (93.5 ha), Cubula (118.6 ha), Cumora (13.6 ha), El Diablo (38.2 ha) and El Siari (190.7 ha). Its grand total measures 8,273 ha.

Figure 4. El Tóbari Bay, Sonora.

Santa María La Reforma Bay

This is a coastal lagoon, located in the central part of the state of Sinaloa, in the eastern Gulf of California, located between 24° 50' and 25° 10' N and 107° 55' and 108° 20' W. It is separated from the Gulf of California by a sandbar that extends from the beach called Isla Altamura, which results in two mouths connecting with the sea at its ends, the first measuring 3.5 km wide and the second 3 km wide. It displays a semidiurnal tidal regime with an annual range of 1.10 m.

Figure 5. Santa María La Reforma Bay, Sinaloa.

MATERIALS

Scales with an accuracy of 1 gr were used, as well as 1 mm precision rulers (ichtyometers), plastic bags, ice coolers, labels, sampling formats, markers, and a freezer.

Information was obtained from various sources:

1. Exhaustive search of published literature on the relationship between SBC and shrimp in different zones: global, the Pacific Ocean, and the Gulf of California. 2. Contents of the daily fishing logbooks, recorded by on-board observers, within the various bays of Guaymas-Empalme, El Tobari, and Bahía de Lobos in Sonora; and in the Bay of Santa Maria La Reforma in Sinaloa, during the Mexican Pacific shrimp fishing season from September to December of 2011.

The fishing gear used in the bays of Sonora were entanglement nets (known as “chinchorro de línea”) with a length of 266 m and with an average height of 75 to 50 mesh-squares. From 2 to 3 of these 3 entanglement nets are used per boat, using different mesh sizes (2", 2 ¼", 2 /8" and 2 ½"). In the state of

Sinaloa, two suripera-type nets were used per vessel, each with a length of 14 m of headline and in mesh sizes between 1 ¼ " and 1 ¾".

Shrimp and SBC were sampled. 5 kg shrimp (with head) samples were collected, and all of the SBC obtained per fishing cast; the name of the capture zone, date, depth, the amount of shrimp caught, and amount of SBC were all recorded. The SBC samples were separated by species and biometry was performed on each organism (Nikolsky, 1963). The taxonomic identification of the species was performed using the keys and descriptions of Jordan and Evermann (1896-1900), Meek and Hildebrand (1923- 1928), Miller and Lea (1976), Eschmeyer et al. (1983), Fischer et al. (1995), Michael (1993), Schneider (1995), Báerez (1996), De la Cruz-Aguero et al. (1997), and Allen and Robertson (2002).

RESULTS

During this study the chinchorro de linea fishing gear was used in the bays of Sonora, and in Sinaloa the gear in use was the suripera net (Santa Maria La Reforma). From 20 to 30% of all fishing hauls had null SBC incidence, which means that only the target species (blue shrimp) was captured, clearly indicating that both types of gear do not capture any SBC in at least a third of their fishing hauls. Regarding the suripera net, SBC catches remain constantly below 2 kg per day; however the chinchorro line captures up to 100 kg of SBC in one day.

• Composition of the incidental catch within all the bays

Fifty-eight species of SBC were identified under this study, belonging to various taxonomic groups, such as fish, elasmobranchs, crustaceans, and mollusks (gastropods), with the dominant group being fish (Table I).

Table I. SBC species found in the artisanal shrimp fishery of the States of Sonora & Sinaloa. ED= discarded species, ER= retained species (co: commercial) and EP= protection status.

Total # of COMMON NAME SCIENTIFIC NAME Weight USE Orgs (Kg)

Brown crab Callinectes bellicosus 3602 2763.96 ER Pacific anchoveta Cetengraulis mysticetus 2381 1192.18 ED Sea catfish Arius spp. 388 421.18 ED Blue crab Callinectes arcuatus 33 394.93 ER Bass Paralabrax maculatofasciatus 34 230.08 ER Dark spot mojarra Eucinostomus entomelas 61 92.37 ER Grunt Haemulopsis elongatus 231 41.75 ED Snail Phyllonotus erythrostomus 53 30.48 ED Rooster fish Nematistius pectorales 170 27.69 ED Green jack caballus 104 25.25 ED Seabass Cynoscion xanthulus 262 23.12 ED Pacific sierra Scomberomorus sierra 76 22.03 ER Dow’s mojarra Eucinostomus dowii 51 19.02 ER kingcroaker Menticirrhus panamensis 143 17.30 ED Shorthead lizardfish Synodus scituliceps 36 14.72 ED Yellowfin jack Hemocaranx leucurus 49 12.89 ED Pacific flagfin mojarra Eucinostomus currani 162 11.23 ER Bullet tuna Auxis spp. 45 10.54 ED Pacific ladyfish Elops affinis 62 9.73 ED Herring Ophistonema spp. 40 8.79 ED Black axillary mojarra Eugerres axilaris 93 7.33 ER Chano croaker Micropogonias megalops 23 7.29 ED Longspine grunt macracanthus 103 6.46 ED Pacific bumper orqueta 56 4.32 ED Silver seabass Isopisthus remifer 47 3.56 ER Mullet Mugil cephalus 50 2.62 ER Peruvian moonfish Selene peruviana 56 2.35 ED

Table I. SBC species found in the artisanal shrimp fishery of the States of Sonora & Sinaloa. ED= discarded species, ER= retained species (co: commercial) and EP= protection status. Continued Total # of COMMON NAME SCIENTIFIC NAME Weight USE Orgs (Kg)

Flounder Etropus spp. 65 2.19 ED Haller’s round ray Urolophus halleri 30 1.78 ED Kelp bass Paralabrax clathratus 9 1.74 ED Silver seabass Cynoscion parvipinis 8 1.60 ED Shovelnose guitarfish Rhinobatos productus 9 1.32 ED Shortjaw Oligoplites refulgens 99 0.56 ED leatherjacket

Anchovy Anchovia macrolepidota 10 0.55 ED Flounder Paralichthys spp. 22 0.41 ED Salema butterfish Peprilus snyderi 5 0.34 ED Ronco croaker Bairdiella icistia 18 0.34 ED Eastern Pacific Albula esuncula 3 0.26 ED bonefish Gulf Mycteroperca jordani 1 0.21 EP, ER Longjaw leatherjacket Oligoplites altus 6 0.20 ED Triggerfish Balistes polylepis 35 0.19 ED Inshore sand Diplectrum pacificum 38 0.17 ED Peruvian mojarra Diapterus peruvianus 1 0.05 ED Pufferfish Sphoeroides annulatus 35 ED Shorthead lizardfish Synodus scituliceps 36 14.60 ED Bichi unidentified species 19 ED Ratón unidentified species 5 ED Snail Melongena patula 3 ER Snapper Lutjanus spp. 7 ER Shining grunt Haemulopsis nitidus 54 ED Dow’s mojarra Eucinostomus dowii ED Pacific spadefish zonatus 3 ED

• Retained bycatch Retained SBC basically consisted of 13 known species consumed regionally and nationally, including: the sand bass (Paralabrax maculatofasciatus), sierra (Scomberomorus sierra), seabass (Cynoscion spp.), mojarra (Eucinostomus spp.), and the swimming crabs (Callinectes bellicosus and C. arcuatus). These species represent 25% of all SBC species. However, in terms of volume they are not abundant, except for the swimming crabs, the sierras, and the mojarras (Table II). These species were retained mainly because of their good acceptance as food and for family consumption rather than for their size, since they were not large. Only rarely do the fishermen sell the SBC, and then, mainly crabs and sierras (Table II).

• Discarded bycatch During the study it was seen that most SBC species were discarded (75%), because they have no commercial value. This SBC is composed mainly of small-bodied, spiny, thin, and not very pleasantly flavored organisms (Table II).

• Globally threatened species found in the SBC During this study a single specimen of a fish commonly known as the gulf grouper (Mycteroperca jordani) was captured, this species is found in the red list (http://www.iucnredlist.org/details/14049/0) under the status of endangered species, mainly due to its slow growth, its age at first , and its incidental capture in the trawling fisheries (Table II).

• Description of retained, discarded, and threatened species per bay Bay of Guaymas-Empalme Table II and Figure 6 show that the dominant species in the Bay of Guaymas is the swimming crab (Callinectes spp.), with 38%, followed by the Pacific anchovy. There were twelve retained species, and all other organisms were discarded. Only one of the species is endangered. It is worth mentioning that only one specimen was captured throughout the study, and it was only within this bay.

Table II. SBC species in the Bahia de Guaymas, common & scientific names. # of orgs= number of organisms, %= percentage, ed= discarded species, er= retained species (co: commercial) and ep= protection status. # of COMMON NAME SCIENTIFIC NAME % ED ER EP Orgs Blue crab Callinectes bellicosus 2183 37.77 Co No Pacific anchoveta Cetengraulis mysticetus 1868 32.32 No Sea catfish Arius spp. 320 5.54 No Grunt Haemulopsis elongatus 216 3.74 No Rooster fish Nematistius pectoralis 144 2.49 No Pacific flagfin Eucinostomus currani 139 2.41 No mojarra

Table II. SBC species in the Bahia de Guaymas, common & scientific names. # of orgs= number of organisms, %= percentage, ed= discarded species, er= retained species (co: commercial) and ep= protection status. Continued # of COMMON NAME SCIENTIFIC NAME % ED ER EP Orgs Green Jack Caranx caballus 104 1.80 No Longspine grunt Pomadasys macracanthus 98 1.70 No Black axillary Eugerres axilaris 93 1.61 No mojarra Pacific sierra Scomberomorus sierra 59 1.02 Co No Pacific bumper Chloroscombus orqueta 48 0.83 No Yellowfin jack Hemocaranx leucuruz 44 0.76 No Herring Ophistonema spp. 40 0.69 No Peruvian moonfish Selene peruvianis 40 0.69 No Pacific ladyfish Elops affinis 37 0.64 No Snail Phyllonotus erythortomus 35 0.61 Co No Swimming crab Callinectes arcuatus 33 0.57 Co No Shorthead lizardfish Synodus scituliceps 33 0.57 No Panama Menticirrhus panamensis 28 0.48 No kingcroaker Haller’s round ray Urolophus halleri 25 0.43 No Silver seabass Isopisthus remifer 24 0.42 Co No Flounder Paralichthys spp. 22 0.38 Co No Dow’s mojarra Eucinostomus dowii 21 0.36 No Shortjaw Oligoplites refulgens 21 0.36 No leatherjacket Chano croaker Micropogonias megalops 20 0.35 Co No Flounder Etropus spp. 13 0.22 No Anchovy Anchovia macrolepidota 10 0.17 No Kelp bass Paralabrax clathratus 9 0.16 No Silver-blue seabass Cynoscion parvipinis 8 0.14 Co No Shovelnose Rhinobathus productus 8 0.14 Co No guitarfish Longjaw Oligoplites altus 6 0.10 No leatherjacket Inshore sand perch Diplectrum pacificum 6 0.10 No Salema butterfish Peprilus snyderi 5 0.09 No

Table II. SBC species in the Bahia de Guaymas, common & scientific names. # of orgs= number of organisms, %= percentage, ed= discarded species, er= retained species (co: commercial) and ep= protection status. Continued # of COMMON NAME SCIENTIFIC NAME % ED ER EP Orgs Mullet Mugil cephalus 3 0.05 Co No Bullet fish Albula esuncula 3 0.05 No Triggerfish Balistes polilepys 3 0.05 Co No Snail Melongena patula 3 0.05 No Paralabrax Spotted sand bass 2 0.03 No maculatofasciatus Dark spot Mojarra Eucinostomus entomelas 1 0.02 No Paloma pompano Trachinotus paitensis 1 0.02 No Gulf grouper Mycteroperca jordani 1 0.02 Co Si Yellow-white Cynoscion xanthulum 1 0.02 Co No seabass Peruvian mojarra Diapterus peruvianus 1 0.02 No

Fig. 6. Composiciónde la FAC en la Bahía de Guaymas. C. arcuatus, 7.67 Arius P.maculatofasci spp, atus, 4.47 8.12 E. C. mysticetus, entomella 22.87 , 1.75

Otros, 5.16

C. bellicosus, 49.82

Figure 6. SBC composition in the Bay of Guaymas, Sonora.

Bahía de Lobos Bay

Table III and Figure 7 show that the dominant species found in Bahía de Lobos Bay is the swimming crab (Callinectes spp.) with 45%. Six species were retained,

corresponding to 25%; the rest of the species were discarded and none of these is threatened. The green crab (Callinectes bellicosus) is the main species of interest because of its size.

Table III. SBC species in Bahia de Lobos, common & scientific names. # of orgs= number of organisms, %= percentage, ed= discarded species, er= retained species (co: commercial) and ep= protection status.

COMMON NAME SCIENTIFIC NAME # of Orgs % ED ER EP Swimming crab Callinectes spp. 1000 45.60 Co No Pacific anchoveta Cetengraulis mysticetus 458 20.88 No Seabass Cynoscion xanthulum 261 11.90 Co No Panama Menticirrus panamensis 115 5.24 No Kingcroaker Shortjaw Oligoplites refulgens 78 3.56 No leatherjacket Bullet tuna Auxis spp. 45 2.05 No Dark spot mojarra Eucinostomus entomelas 42 1.92 No Sea catfish Arius spp. 34 1.55 No Roosterfish Nematistius pectoralis 26 1.19 No Flounder Etropus spp. 23 1.05 No Mullet Mugil cephalus 18 0.82 Co No Peruvian moonfish Selene peruviana 16 0.73 No Paralabrax Spotted sand bass 10 0.46 Co No maculatofasciatus Pacific sierra Scomberomorus sierra 10 0.46 Co No Pacific ladyfish Elops affinis 8 0.36 No Pacific bumper Chloroscombus orqueta 8 0.36 No Ronco croaker Bairdiella icistia 5 0.23 No Longspine grunt Pomadasys macracanthus 5 0.23 No Yellowfin jack Hemicaranx leucurus 5 0.23 No Haller’s round ray Urolophus halleri 5 0.23 No Pacific spadefish Chaetodipterus zonatus 3 0.14 No Chano croaker Micropogonias megalops 3 0.14 Co No Shorthead Synodus scituliceps 3 0.14 No lizardfish Shovelnose Rhinobathus productus 1 0.05 Co No guitarfish Pufferfish Sphoeroides annulatus 11 0.50 Co No

Fig. 7.- Composición de la FAC en Bahía de Lobos, Son. M. panamensis 5% O. refulgens C. xanthulum 4% 12% Auxis spp C. mysticetus 2% 21% Otros 11%

Callinectes spp 46%

Figure 7. SBC composition in Bahía de Lobos, Sonora.

Bahia del Tobari

Table IV and Figure 8 show that the dominant species at El Tobari Bay is the swimming crab (Callinectes spp.) with 72%. Six other species were retained, corresponding to 55%; the rest of the species were discarded, with none listed as threatened.

Table IV. SBC species in the Bahia del Tobari, common & scientific names. # of orgs= number of organisms, %= percentage, ed= discarded species, er= retained species (co: commercial) and ep= protection status. # of COMMON NAME SCIENTIFIC NAME % ED ER EP Orgs Swimming crab Callinectes spp. 419 71.99 Co No Pacific anchoveta Cetengraulis mysticetus 55 9.45 No Dow’s mojarra Eucinostomus dowii 30 5.15 No Mullet Mugil cephalus 29 4.98 Co No Snail Phyllonotus erythortomus 18 3.09 Co No Mojarra Eucinostomus entomelas 18 3.09 No Pacific sierra Scomberomorus sierra 7 1.20 Co No Snapper Lutjanus spp. 6 1.03 Co No

Fig. 8. Composición de la FAC en Bahía del Tobari

P. erythortomus 3% C. mysticetus M. cephalus 10% E. dowii 5% 5% E. entomella 3% Otros 5% Callinectes spp S. sierra 72% 1% Lutjanus spp 1%

Figure 8. SBC composition in Bahia del Tobari, Sonora.

Santa María La Reforma Bay

Table V and Figure 9 show that the dominant species observed in this bay was the grunt or the triggerfish with 15.7%. There were 4 retained species, the rest of the species were discarded, and none were listed as threatened.

Table V. SBC species in the Bahia Santa Maria-La Reforma, common & scientific names. # of orgs= number of organisms, %= percentage, ed= discarded species, er= retained species (co: commercial) and ep= protection status. # of COMMON NAME SCIENTIFIC NAME % ED ER EP Orgs Grunt Haemulopsis nitidus 54 15.74 No Sea catfish Arius spp. 34 9.91 No Triggerfish Balistes polylepis 32 9.33 Co No Inshore sand perch Diplectrum pacificum 32 9.33 No Flounder Paralichthys spp. 29 8.45 No Pufferfish Sphoeroides annulatus 24 7.00 Co No Silver seabass Isopisthus remifer 23 6.71 Co No Mojarra Eucinostomus currani 23 6.71 No Paralabrax Spotted sand bass 22 6.41 Co No maculatofasciatus Bichi Unidentified species 19 5.54 No Pacific ladyfish Elops affinis 17 4.96 No Panama kingcroaker Haemulopsis elongatus 15 4.37 No Ronco croaker Bairdiella icistia 13 3.79 No Ratón Unidentified species 5 1.46 No Snapper Lutjanus spp. 1 0.29 Co No

Fig. 9.- Composición de la FAC en La Reforma, Sin. I. remifer, 6.71 E. currani, 6.71 P. S. annulatus, maculatofasciat 7.00 us, 6.41 Paralichthys spp, 8.45 bichi, 5.54

Otros, 14.87 D. pacificum, 9.33 B. polylepis, H. nitidus, 15.74 9.33 Arius spp, 9.91

Figure 9. SBC composition in La Reforma, Sinaloa.

Proportion of incidental catches For the duration of this study, information was obtained from a total of 854 fishing hauls working within the study site. On average there were 210 fishing hauls per bay, with a null-SBC amount of hauls of 20-30% (average of bays), in which the only species captured was shrimp.

The analysis of the ratio of average shrimp to SBC in all the bays was of 1:0.4, although this ratio varied between bays. Ratios per bay are shown in tale See Table VI.

Table VI. Shrimp to SBC proportion by bay, during the 2011 shrimping season. Locality Proportion (Shrimp:SBC) Bay of Guaymas 1 : 0.50 Bahía de Lobos Bay 1 : 0.28 El Tobari Bay 1 : 0.49 La Reforma Bay 1 : 0.50

DISCUSSION

The artisanal shrimp fisheries’ bycatch in Mexico has been little studied, with the exception of Amezcua et al. (2006) and Suenaga (2010) who conducted studies on the effects of artisanal fishing, and their results are an important reference for this study, given the scarcity of available literature. Nonetheless, there are several studies about the offshore shrimp trawling fishery, which is conducted by larger vessels, and several studies report that the proportion of shrimp to SBC averages 1:10 kg (Alverson et al. 1996, García and Gómez 2000, Lopez-Martinez et al. 2005, Morales-Azpeitia 2011). Therefore, the shrimp trawling fishery is regarded worldwide as one of the highest SBC capture fisheries (Kelleher 2005, Gillett 2010). The SBC generated by these fishing vessels, by zones, is highly variable (Arvizu and Chavez 1972, Chapa 1976, Pérez-Mellado 1980, Yañez-Arancibia 1984, Villaseñor-Talavera 1997), even between seasons within the same area (Pérez-Mellado 1980, Grande-Vidal and Diaz-Lopez 1981, Villaseñor- Talavera 1997, Pérez-Mellado 1998, Lopez-Martinez et al. 2007).

While it is true that in terms of engineering the several types of fishing gear used throughout the world all have the ability to capture incidental fauna, which is allowed up to a certain percentage, it is highly relevant that this study found a high percentage of null-SBC fishing hauls (20-30%) in the bays of Sonora, when the chinchorrode linea was being used. This means that at least one third of the hauls performed using this shrimp fishing gear did not capture any SBC, and in terms of the negative impacts upon the communities of marine and coastal lagoon ecosystems, these are nonexistent. Another benefic factor for the marine ecosystem, in terms of the extraction of natural resources, is that this activity does not take place throughout the year, occurring during only four months (September to December). However, SBC was captured during the artisanal shrimp fishing operations in all of the bays and months of duration of this present study, and these ranged in average between 1:0.2 to 1:1 (shrimp:SBC). This figure is eight times lower than the proportion of SBC generated using shrimp trawling boats (García-Caudillo and Gómez-Palafox 2005, Morales-Azpeitia 2011).

The proportion of shrimp SBC in this study was lower than that reported by other authors for this same fishery. Amezcua et al. (2006) found a ratio of 1:15 in the La Reforma lagoon system and Suenaga (2010) reported a ratio of 1:22 for the Bay of Guaymas. The high proportion of shrimp SBC reported by Amezcua et al. may be due to the fact that sampling was conducted between December 2001 and May 2002, a period in which shrimp abundances are either too low or next to zero. In the case of Suenaga’s study, even when the work was done throughout the 2003-2004 shrimp fishing season, shrimp catches had a very low yield, since these were obtained from just a single fishing vessel. It is worth mentioning that for the duration of the commercial shrimp fishery the best fishing zones are always actively sought, and fishing areas known to yield SBC are avoided (for example, in to avoid the capture of the sea catfish/chihuil (Arius spp.)) and a fishermen’s experience plays a very important role in this.

With respect to the composition of the SBC, within all bays 46 species were identified during the present study, but only 10 were identified at the genus level (such as Paralichthys, Lutjanus, and Etropus), but

these do not represent a volume any greater than 1% of the total catch. The number of species found in this study were higher than those reported by Suenaga (2010), who reported 44 species just in Guaymas. The difference may be due to the higher number of bays studied.

The most diverse group was fish, but the dominant SBC species, in terms of volume, was the swimming crab (Callinectes spp.).

As to the SBC species retained by bay, on average this represents 25% of the total of species. These species are mainly intended for family consumption, except when volumes are higher (over 20 kg) and only if there is a buyer present then it is marketed; the swimming crabs, the Pacific sierra, and the corvina are the main species in this category. Of all SBC species, 75% are discarded (Table II).

In Sonora, particularly, the fishing effort has increased by 83% in just a decade (1980–1990), yet shrimp catches are decreasing. The most outstanding point about this situation is the decrease of the fishing season itself — ever since 1981–1986 the shrimping season lasted until February, according Padilla- Serrato (2005), and during this study, the season was reduced to end in December, which, according to Hernandez-Carballo and Macias (1996), has been the norm since the 1991–1992 season.

The coastal shrimp fishery has had an increase in its fishing efforts and these may cause socio-economic deficiencies. These are due to the variation in shrimp pricing during the fishing season or can be explained by an increase in the yield of larger-sized organisms, which command higher prices on the international markets (Cruz-Romero et al. 1996).

The shrimp resource has been strongly and consistently exploited, both in the artisanal zone and at high sea, thus it is said to be on the verge of a collapse (Wadsworth 1976). It is said that this problem is due to the elaboration of sophisticated models and to a prolonged capture of time classes, resulting in overexploitation. Two of the biggest problems in the collapse of this fishery may be due to the effect of unaccounted externalities; one of these is the stock’s externality, which may cause capture declines, which can be accounted for by the entry of new vessels to the fishery that have casued a reduction of the resource to existing fishermen and thus increase the fishing costs. This is commonly observed not only in the Guaymas area, but also in other areas and is due to incorrect fisheries management and to a lack of supervision that allows the introduction of hundreds of boats that only capture this resource during the first fishing days of the season. Another possible factor could be the increase and agglomeration of boats within a fishing area, which results in a reduction of the fishing area under which the fishing effort is not successfully applied (Seijo et al. 1997, Flores Olivares 2003).

CONCLUSIONS AND RECOMMENDATIONS • The impacts of the artisanal blue shrimp fishery are low, both in terms of catch volumes of SBC and the number of species caught, and can be summarized under four main factors:

1. A third of the fishing hauls made in the bays and coasts were null (SBC was not captured), which reduces the impact of fishing on the ecosystem. 2. The average proportion shrimp to SBC in this study was 1:0.5. 3. The fishing season is only four months long (September to December). 4. SBC volumes captured using the suripera net are less than 2 kg per fishing day.

• The SBC’s retained species per bay is on average a 25% of the total of species caught. These species are used mostly for home consumption and some are marketed, such as the crab, sierra, and corvina.

• Most of the SBC species are discarded (75%).

• Of the total number of captured species, only a single specimen of one species (Mycteroperca jordani), considered as under special protection, was found within the bay of Guaymas-Empalme.

• This study should be continued for several fishing seasons, in order to strengthen the results and analyze the population dynamics of the dominant SBC species, thus helping to determine the health status of these populations which may be indicative of impacts.

• Fishing gear verification is recommended, mainly on the gillnets as their design and construction characteristics are beyond those established under the Mexican Official Standards Policy (NOM). The use of authorized fishing gear guarantees a lower impact on bycatch.

• It is recommended to perform studies on both intraspecific and multispecies selectivity, in order to increase the fishing efficiency of this type of gear.

List of participants

Jesús Guadalupe Padilla Serrato, M.Sc. (Bahía Guaymas-Empalme) Everardo Miranda Mier, Fisheries Technician (Bahía Guaymas-Empalme) Alejandro Valdez Pelayo, M.Sc. (Bahía de Lobos) Marina Estefanía García González, B.Sc. (Bahía de Lobos) José Francisco Cueto Moreno, B.Sc. (Bahía el Tobarí) Tomás Sánchez y Ramón (Bahía Santa María La Reforma)

Also, we wish to thank the fishermen who supported the study and provided information about their daily fishing activities.

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