Importance of Bahia Sebastian Vizcaino As a Nursery Area for White

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Fisheries Research 188 (2017) 125–137

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Original research article

Importance of Bahia Sebastian Vizcaino as a nursery area for white

sharks (Carcharodon carcharias) in the Northeastern Paciﬁc: A ﬁshery

dependent analysis

a a,∗ a

Erick C. Onate-González˜ , Oscar Sosa-Nishizaki , Sharon Z. Herzka ,

b b a c

Christopher G. Lowe , Kady Lyons , Omar Santana-Morales , Chugey Sepulveda ,

d a e

César Guerrero-Ávila , Emiliano García-Rodríguez , John B. O’Sullivan

Department of Biological Oceanography, CICESE, Carretera Ensenada-Tijuana #3918, Zona Playitas, Ensenada, BC, Mexico

Department of Biological Sciences, California State University, Long Beach, CA, USA

Pﬂeger Institute of Environmental Research, Oceanside, CA, USA

Terra Peninsular A.C., Ensenada, Baja California, Mexico

Monterey Bay Aquarium, Monterey, CA, USA

a r t i c l e i n f o a b s t r a c t

Article history: In the Northeastern Paciﬁc, immature white sharks (Carcharodon carcharias) have been recorded in the

Received 18 August 2016

nearshore waters of the Southern California Bight (SCB), USA, along the Mexican coast off Baja California

Received in revised form

and throughout the Gulf of California, which makes them susceptible to incidental capture by coastal

17 December 2016

ﬁsheries. While the SCB is considered a nursery area for white sharks, records of young-of-the-year white

Accepted 19 December 2016

sharks (YOY) in Bahia Sebastian Vizcaino (BSV) off central Baja California suggest that this region could

Handled by Prof. George A. Rose

also be an important white shark nursery area, but a formal evaluation of the region’s habitat function

is lacking. We analyzed incidental catch records of white sharks from the US-Mexico border to BSV and

Keywords:

evaluated whether Heupel et al.’s (2007) criteria for the identiﬁcation of shark nursery areas were met

White shark

for BSV. We compiled a total of 390 white shark incidental catch records between 1999 and 2013 and

Nursery area

Incidental catch compared incidental catch records from the region north of Bahia Sebastian Vizcaino (NBSV; an area

Fisheries not considered to be a nursery ground) with those for BSV. There was a signiﬁcantly higher abundance

Bahia Sebastian Vizcaino of newborns and YOY in BSV than NBSV. White shark were caught consistently throughout the year

within BSV; however, the majority (70.1%) were caught between May and September. Our results are

consistent with the shark nursery area criteria proposed by Heupel et al. (2007), and indicate the region

between BSV to the SCB may be an important migration corridor for YOY and juvenile white sharks.

Future management and conservation efforts ought to consider BSV’s nursery habitat function.

1. Introduction speciﬁc geographic areas that are essential for the preservation of

threatened or endangered species (critical habitat) are important

Juvenile shark survivorship is partially dependent upon the steps for the conservation and sustainable long-term management

availability of suitable nursery areas (Yates et al., 2012; Ward-Paige of shark populations (Heithaus, 2007). Successful management and

et al., 2015). Identifying shark nursery areas and documenting the conservation of shark populations is dependent upon implement-

ing strategies that are conducive to successful juvenile recruitment

and survivorship.

Nearshore habitats such as bays and estuaries are highly pro-

Abbreviations: BSV, Bahia Sebastian Vizcaino (Mexico); CONAPESCA, National

Commission of Fisheries and Aquaculture (translated from Spanish); JWS, juve- ductive, have a relatively high abundance and diversity of species,

nile white sharks with sizes ranging from 175 cm to 300 cm in total length; NBSV, some of them important for ﬁsheries, and support large abundances

North of Bahia Sebastian Vizcaino (region that extends from the Popotla to Punta

of juvenile shark species, many of which utilize different habitats

Canoas ﬁshing camps along the western coast of the Baja California peninsula); NEP,

than those of adults (Dahlgren et al., 2006; Knip et al., 2010). As

Northeastern Paciﬁc; NWS, newborn white sharks less than 150 cm total length;

a result, these areas are often heavily targeted by ﬁshers, and can

SCB, Southern California Bight (USA); SDS, selected demersal species that comprise

species that are caught with bottom gillnet ﬁshing gear; YOY, young-of-the-year often be degraded due to coastal development, storms and other

white sharks ranging from neonates to 175 cm total length.

anthropogenic impacts. Potential nursery areas for sharks were ∗

Corresponding author.

ﬁrst identiﬁed based on the presence or absence of young individ-

E-mail addresses: [email protected], [email protected] (O. Sosa-Nishizaki).

http://dx.doi.org/10.1016/j.ﬁshres.2016.12.014

126 E.C. O˜nate-González et al. / Fisheries Research 188 (2017) 125–137

uals (Springer, 1967). Castro (1993) proposed that for aplacental of genetic differences between immature sharks sampled in the

viviparous sharks, nursery areas could be inferred based on the SCB and Bahia Sebastian Vizcaino (BSV), Mexico, located in the

presence of gravid females, neonates and small juveniles. How- Paciﬁc off the central Baja California peninsula (Onate-González˜

ever, not all species have discrete nursery areas, as some species et al., 2015). Given the limited number (<100) of individuals sam-

spend all life stages in the same area while others are more tran- pled by Onate-González˜ et al. (2015), and the present-day lack of

sient (Knip et al., 2010). Hence, the mere presence of gravid females nuclear DNA data that provides information on bi-parental inher-

or immature sharks in a particular habitat does not always indi- itance, the level of population connectivity between sharks found

cate that the habitat is actually function as a nursery area (Heupel in the SCB and Mexican waters has not been well established.

et al., 2007). Bass (1978) suggested that immature sharks might The white shark is recognized as a species vulnerable to over-

require two distinct types of nursery areas depending on their size exploitation by the International Union for Conservation of Nature

and life stage: a primary nursery area is where sharks are born and (IUCN) Red List (Hilton-Taylor, 2000), and it has been included in

spend the ﬁrst part of their lives, and a secondary nursery area is Appendix II of the Convention on International Trade in Endangered

that which is inhabited by the slightly older, but not yet mature Species of Wild Fauna and Flora (CITES) since 2004. In Mexico, the

individuals. Recently, Heupel et al. (2007) argued that this deﬁ- white shark has been designated as a “threatened species” through

nition was ambiguous and that nursery types proposed by Bass ofﬁcial regulations NOM-059-SEMARNAT-2001 (DOF, 2002, 2010)

(1978) were difﬁcult to deﬁne geographically, as primary and sec- and NOM-029-PESC-2006. The latter established the prohibition

ondary nurseries can spatially overlap. For example, neonates born of intentional catch, retention and commercialization of any body

in the primary nursery area can move to another region and sub- part of this species (DOF, 2007). Since 2012, a shark and ray ﬁshing

sequently return to the same area, which would then function as a closure has been established in Mexican waters between May 1st

secondary nursery. For this reason, Heupel et al. (2007) proposed and July 31th to protect a fraction of the reproductive stock of com-

the elimination of the terms “primary” and “secondary” and sug- mercially important elasmobranch species (DOF, 2012). Although

gested that the term “nursery area” should be used to collectively the protection of white sharks was not the speciﬁc purpose of this

represent these critical habitats. They also proposed the follow- regulation, the timing of this closure likely aids in the protection of

ing three criteria for identifying nursery areas for newborns and this species since it coincides with the time of year during which

young-of-the-year sharks: 1) the area must have a higher relative JWS are found close to shore along the western coast of Baja Califor-

abundance of neonates and young juveniles compared to other nia (Santana-Morales et al., 2012). Since February 2014, a complete

areas; 2) immature sharks must show the tendency to remain or ﬁshing ban for white sharks and the mandatory release of inciden-

return to the area for extended periods; and 3) the area should be tal catches has been established in Mexican waters (DOF, 2014).

consistently used by immature sharks across years. Based on this Despite the protective regulations that have been implemented

deﬁnition, all three criteria must be met for a particular area to be internationally and by Mexico, the incidental catch of this species

considered as shark nursery habitat (Heupel et al., 2007). still occurs in commercial and recreational ﬁsheries (Malcolm et al.,

The white shark (Carcharodon carcharias) is an apex preda- 2001; Dudley and Simpfendorfer, 2006; Lowe et al., 2012; Santana-

tor with size-at-birth between 120 and 150 cm total length (TL) Morales et al., 2012; Dicken and Booth, 2013; Lyons et al., 2013;

(Francis, 1996), and grows to a maximum length of 610 cm TL Curtis et al., 2014). This continued pressure supports the need to

(Castro, 2012). Four different life stages have been proposed based assess their population status, ﬁshery interaction rates, and identify

on size and reproductive stage: 1) young-of-the-year (YOY) sharks critical habitats, including nursery areas.

ranging from newborn size (120 cm–150 cm TL) to 175 cm TL; 2) Based on the size distribution and seasonality in catch records,

juvenile (JWS) sharks ranging from 175 cm to 300 cm TL; 3) sub- Klimley (1985) proposed that the SCB was a parturition and nursery

adult sharks that include individuals >300 cm to maturity; and 4) area for white sharks, and reported that adult white sharks were

adult, mature sharks that are >360 cm TL in the case of males most frequently seen and caught in central and northern Califor-

and >480 cm TL for females (Cailliet et al., 1985; Francis, 1996; Pratt, nia during September to December, and that YOY were only caught

1996; Wintner and Cliff, 1999; Malcolm et al., 2001; Martin et al., south of Point Conception during the summer. More recently, JWS

2005). White sharks are mainly found in tropical and temperate have been well documented in nearshore waters between Point

oceans at relatively natural low population densities and their dis- Conception, California, and BSV in Baja California (Weng et al., 2007;

tribution varies based on their size (Compagno et al., 2005). Adult Domeier, 2012; Lowe et al., 2012; Santana-Morales et al., 2012).

white sharks aggregate around oceanic islands that typically har- Artisanal and industrial ﬁsheries on the west coast of Baja California

bor pinniped colonies, while YOY and JWS are primarily distributed target coastal and pelagic elasmobranchs, bony ﬁshes and inverte-

close to shore (at depths <200 m) (Weng et al., 2007; Domeier, brates using a variety of ﬁshing gears (Sosa-Nishizaki et al., 2008;

2012; Lowe et al., 2012; Ebert et al., 2013). Cartamil et al., 2011). Santana-Morales et al. (2012) documented

In the Northeastern Paciﬁc (NEP), YOY, JWS and sub-adults the incidental catch of YOY and juvenile white sharks along the

primarily inhabit nearshore waters off California and the Baja Cali- Paciﬁc coast of Baja California during 1999 and 2010. Eighty-three

fornia peninsula (Cailliet et al., 1985; Klimley, 1985; Malcolm et al., white sharks (74.7% of the total) were caught by artisanal bottom-

2001; Weng et al., 2007; Santana-Morales et al., 2012; Lyons et al., gillnets, leading them to suggest that the continental shelf is an

2013). Based on electronic tagging studies, it has been shown that important habitat for YOY and JWS, and that BSV could serve as an

some immature white sharks (>165 cm TL) move along the coast important nursery area.

from the Southern California Bight (SCB), US, to Mexican waters In this study, we use a robust conceptual framework with spe-

off Baja California and sometimes into the Gulf of California (Weng ciﬁc criteria to identify nursery habitats as deﬁned by Heupel et al.

et al., 2007; Weng et al., 2012). However, given the short retention (2007) in order to evaluate the function of BSV as white shark nurs-

of most satellite tagging deployments to date (less than 3 months), ery area. We compiled all artisanal ﬁshery-dependent catch data

only one YOY returned to the SCB following its southern migration to date of immature white shark catches off the western coast of

(Weng et al., 2007; J. O’Sullivan, pers comm). Using acoustic tags, ﬁve northern Baja California for 1999–2013, leading to the most com-

juvenile white shark tagged at SCB were detected inside Laguna plete YOY and JWS data set compiled for northwestern Mexico.

Ojo de Liebre (Mexico) in the acoustic receivers array and some- Information about white shark nursery habitat could be used to

time after they were detected at SCB (Lowe and Sosa-Nishizaki, improve protection and reduce mortalities associated with com-

pers obs). Mitochondrial DNA analyses, which provide information mercial ﬁsheries.

on maternally inherited genetic traits, have indicated the existence

E.C. O˜nate-González et al. / Fisheries Research 188 (2017) 125–137 127

2. Materials and methods Popotla to Pta. Canoas) or within BSV (Fig. 1). The size frequency

distributions of white sharks caught in those two regions were

2.1. Study area compared using a Kolmogorov-Smirnov two-sample test analysis.

The seasonality of the catch-records was qualitatively compared

The Paciﬁc waters off the Baja California peninsula are located between 2011 and 2012, and compared with the Santana-Morales

in the southern portion of the California Current System. At Punta et al. (2012) results.

Eugenia, the California Current meets a warmer current from the

south, creating a complex oceanographic region that is a well-

2.4. Relationship between white shark incidental catches and

documented biogeographical transition zone (Dawson et al., 2006;

landings of select demersal species

Durazo, 2015). Punta Eugenia represents the southern limit of the

distribution of many ﬁsh taxa common to the San Diegan Bio-

Estimating white shark relative abundance using a catch per

geographical Province, and the northern limit for many ﬁsh taxa

unit effort (CPUE) index was not possible due to the lack of ﬁshing

common to the tropical Panamic Province (Horn et al., 2006).

effort data. As a CPUE proxy we, therefore, analyzed the number of

BSV is a large embayment (35,678 km ) with Punta Canoas as

white sharks caught incidentally within BSV relative to the tonnage

the northernmost point and Punta Eugenia as its southernmost

of ﬁsh reported at the Mexican National Commission of Fisheries

point (Cartamil et al., 2011) (Fig. 1). The continental shelf is broader

and Aquaculture (CONAPESCA) ofﬁces associated with BSV. Even

toward the south of BSV and reaches a maximum width of 140 km 2

though BSV covers a large area (35,678 km ), we used information

close to the central part of the embayment (Cartamil et al., 2011).

from Jesus Maria and Guerrero Negro ofﬁces only (Fig. 1), because

The average depth is 75 m with a maximum of 100 m in the central

ﬁshermen are mostly based in ﬁshing camps along the southern

region and 200 m in the northeastern outer part of the embayment

portion of the bay (Laguna Manuela and Las Casitas), and they

(Fig. 1). Like the SCB (Dailey et al., 1993; Allen et al., 2007), BSV is

mainly operate in waters close to the mouth of Laguna Ojo de Liebre

one of the most productive areas in the NEP due the presence of a

or within the lagoon (Fig. 2) (Guerrero-Ávila et al., 2013).

seasonal anticyclonic gyre, shallow waters, coastal topography, and

Because Santana-Morales et al. (2012) reported that around

prevailing regional wind patterns that are conducive to regional

75% of incidental catches were caught with bottom gillnets, we

upwelling (Mancilla-Peraza et al., 1993; Amador-Buenrostro et al.,

focused on landings of selected demersal species (SDS) that are

1995). The embayment is characterized by high primary productiv-

actually caught with this ﬁshing gear. SDS includes ﬂounders

ity, which is concentrated and retained within the bay and supports

(Paralichthys sp, and Pleuronichthys sp), bat rays (Myliobatis sp), dia-

high relative abundances of consumers compared to the northern

mond stingray (Dasyatis sp), shovelnose guitarﬁsh (Rhinobatos sp,

region of Baja California (Lluch-Belda, 2000).

and Zapteryx sp), angel shark (Squatina californica), small sharks

(different species, locally named “cazón”), and smooth-hounds

2.2. Data sources of white shark incidental catches

(Mustelus sp). To evaluate the monthly variations in incidental

white shark catches, we examined the incidental catches registered

We compiled and analyzed white shark incidental catch records

between June 2011 and May 2012 (corresponding to the period

from 1999 to 2013. The Santana-Morales et al. (2012) database

of the most intense survey effort). SDS landings were pooled by

was re-analyzed to reﬂect incidental catches from 1999 to 2010

month to produce a single series of landings, and compared with

that were registered in artisanal ﬁshing camps located along the

the number of white shark incidental catches.

western coast of Baja California and records from commercial drift

gillnet ﬁshing vessels based out of Ensenada (Fig. 1; Table 1). From

2.5. Bahia Sebastian Vizcaino consideration as nursery area

May 2011 to December 2013, we conducted new monthly sur-

veys of artisanal ﬁshing operations at camps where most ﬁshing

To evaluate whether there was evidence to support Heupel et al.

uses bottom gillnets (Ensenada, San Martin island-San Quintin,

(2007)’s three main criteria for considering BSV a nursery area, we

Santa Rosaliita, Laguna Manuela and Las Casitas; Fig. 1); these ﬁsh-

examined whether 1) YOY were recorded at a higher frequency at

ing camps were also surveyed by Santana-Morales et al. (2012).

BSV compared to NBSV, 2) if there was seasonality in the incidental

Survey visits lasted two to three days per camp. Fishermen log-

catches along the western coast of Baja California, and particularly

book data from the same camps were also analyzed. To maximize

within BSV, and 3) whether incidental catch records were consis-

the number of white sharks recorded outside of the surveys, the

tent across years.

person in charge of recording landings at each ﬁshing camp was

trained in identifying and measuring white sharks. Local ﬁsher-

men independently documented half of the white shark records 3. Results

that took place during the absence of scientiﬁc personnel. When

whole white sharks were identiﬁed, individuals were sexed and the 3.1. White shark incidental catches

total length was measured to the nearest cm. During 2013, survey

effort diminished due to the lack of access we were given to log- We compiled a total of 390 white shark incidental catch records

book data following a gill net ﬁshery ban that went into effect for along the western coast of Baja California from 1999 to 2013. Due to

part of the year. Hence, surveys were only performed in April, May, limited surveying efforts, the records between 1999 and 2005 were

September and November and efforts were concentrated on the sporadic and no more than six white sharks were recorded in any

ﬁshing camps located within BSV (Santa Rosaliita, Laguna Manuela one year (Table 1). Although the number of records increased dur-

and Las Casitas). ing 2006, this was due to the tallying of carcasses observed during

discard site surveys as reported by Santana-Morales et al. (2012).

2.3. Incidental catch analysis Only six white sharks were actually reported as caught in 2006.

From 2007–2010 the number of white sharks ﬂuctuated between

To characterize temporal and size-based catch patterns, 10 and 25 sharks per year. White shark-speciﬁc surveys led to 167

white sharks were divided into three categories: newborns records in 2011, 93 in 2012, and only 7 in 2013 (Table 1).

(NWS: <150 cm TL), YOY (150–175 cm TL), and JWS (175–300 cm Total length was measured for 91.8% of all carcasses (n = 353;

TL) (Francis, 1996). Fishing camps were grouped based on whether range 118–300 cm TL). The size-frequency distribution presented

the camps were located north of Bahia Sebastian Vizcaino (NBSV; two peaks at the 135–140 cm and 170–175 cm TL size classes. Based

128 E.C. O˜nate-González et al. / Fisheries Research 188 (2017) 125–137

Fig. 1. Fishing camps and main ﬁshing ofﬁces (denoted by *) where landings records come from. (1) Popotla, (2) Ensenada, (3) Pto. Santo Tomas, (4) Pta. San Jose, (5) Erendira,

(6) San Quintin, (7) El Rosario, (8) Pta. Canoas, (9) Pta Cono, (10) Pta. Maria, (11) Sta. Rosaliita, (12) Pta Rosario, (13) Jesus Maria, (14) Guerrero Negro, and (15) Isla Cedros.

NBSV = north Bahia Sebastian Vizcaino region.

Table 1

Annual records of incidentally caught white sharks, specifying the type of record as discarded head (DH), logbook data (LD), landing sampling (LS), on-board record (ObR) or

fresh head (FH).

Year #White sharks Kind of survey Kind of effort

1999 1 DH Recorded at a discard site

2000 1 LD From a drift-gillnet vessel

2001 2 LD From a drift-gillnet vessel

2002 2 LD From a drift-gillnet vessel

2003 – – No survey effort

2004 6 DH Recorded at a discard site

2005 – – No survey effort

2006 56 DH, LS, LD, ObR Survey of discard site, landings sites and records from drift-gillnet

vessel

2007 8 LS Survey at ﬁshing camp

2008 25 DH, LS, FH Survey of discard and landings sites

2009 12 LS, LD Survey at ﬁshing camp and records from drift-gillnet vessel

2010 10 LS Survey at ﬁshing camp

2011 167 DH, LS, LD White shark speciﬁc surveys at discard sites, landing sites and records

from artisanal pangas

2012 93 DH, LS, LD White shark-speciﬁc surveys at discard sites, landing sites and records

from artisanal pangas

2013 7 DH, LS, LD White shark-speciﬁc surveys at discard sites, landing sites and records

from artisanal pangas

on their size, 135 sharks were categorized as NWS, 166 as YOY and indicated signiﬁcant differences (KS: 0.639; p < 0.01), which was

52 as JWS (Fig. 3). driven by differences in the proportion of size classes between

Of the 353 sharks that were measured, 94% were caught within regions [KS: 0.46 (NWS), 0.45 (YOY), 0.66 (JWS); p < 0.01 (for all)].

BSV and the other 6% were landed north of Pta. Canoas (NBSV; Newborns, YOYs and JWS were caught most months but the

Fig. 4). Of the 333 white sharks sampled within BSV, 40% were highest numbers were recorded between May and September

categorized as newborns, 49% as YOY and 11% as JWS (Fig. 3). (Fig. 5). Newborn white sharks were mostly caught during June

Kolmogorov-Smirnov two-sample test analysis of the size fre- and July. YOYs were caught during most months, except March

quency distributions of white sharks caught in NBSV and BSV and April (Fig. 5). The 170–175 cm TL size class predominated from

E.C. O˜nate-González et al. / Fisheries Research 188 (2017) 125–137 129

Fig. 2. Map of the bottom set gillnet ﬁshing area in Bahia Sebastian Vizcaino as reported by Guerrero-Ávila et al. (2013). Lines represent depths and contours represent

percentage of use of gillnets.

May to November (n = 106; Fig. 6) and represented 32% of all sharks landed primarily during April through October. In 2012 landings

caught inside the bay. Almost all young sharks were recorded dur- peaked in May (23 t), even though the seasonal closure started that

ing the intensive surveys conducted in 2011 and 2012 (except for year. There were no landings reported in May and June after 2012

one of 172 cm TL caught in 2008). (Fig. 7), as expected due to the seasonal closure. Shark landings did

not show a consistent temporal pattern, although winter months

had lower landings. While during some years landings peaked in

3.2. Relationship of white shark incidental catch with selected

June and July, maximum values were documented in April and

demersal species (SDS) ﬁshing landings

November in other years. During 2012 and 2013, high shark land-

ings were documented in March and April and from August through

According to CONAPESCA, the largest landings of SDS ﬁsheries

October, reaching levels of around 10 t per month.

for the period of 2008–2013 were comprised of the batoids (mainly

The consistent ﬂounders, batoids and shark landings across

the shovelnose guitarﬁsh group) with an average annual catch of

months (Fig. 7), indicated that artisanal ﬁshing operations inside

116 t, followed by ﬂounders with 103 t (Table 2). Most ﬂounder

BSV used bottom gillnets throughout the year. Fig. 8a shows the

landings took place between February and August with a peak in

monthly number of white sharks incidentally caught at BSV and

April, May or July, depending on the year. Monthly catches ranged

the SDS catches landed during the period in which intense surveys

between 17 and 40 t (Fig. 7). Between 2008 and 2011, batoids were

130 E.C. O˜nate-González et al. / Fisheries Research 188 (2017) 125–137

Fig. 3. Size-based frequency histogram of white sharks recorded as incidental catch along the western coast of Baja California from 2004 to 2013. Development stages are

indicated (NWS = newborn; YOY = young of the year; JWS = juvenile).

Fig. 4. Frequency histogram of white shark stage classes recorded as incidental catch north of Bahia Sebastian Vizcaino (NBSV) region and within Bahia Sebastian Vizcaino

(BSV) nursery from 2004 to 2013. NWS = newborn; YOY = young of the year; JWS = juvenile.

Fig. 5. Size-based histogram of the number of white sharks caught incidentally in Bahia Sebastian Vizcaino from 2004 to 2013. Newborn (<150 cm TL); YOY (young-of-the-year

−

150–175 cm TL); Juvenile (175–300 cm TL).

E.C. O˜nate-González et al. / Fisheries Research 188 (2017) 125–137 131

Fig. 6. Monthly frequency histogram of YOY white sharks with sizes 170–175 cm TL recorded as incidental catch in Bahia Sebastian Vizcaino from 2008 (n = 1) and 2011–2012

(n = 105).

Table 2

Annual total landings (tonnes) of select demersal species (SDS) caught by bottom gillnets as reported in the CONAPESCA ﬁshing ofﬁces of Jesus Maria and Guerrero Negro

(pooled) in the Bahia Sebastian Vizcaino region from 2008 to 2013 (CONAPESCA, 2014). Bold values represent totals.

2008 2009 2010 2011 2012 2013 Total

TOTAL Flounders 123.8 127.7 87.7 78.0 75.3 124.7 617.1

Bat eagle ray (Myliobatis sp) 0.8 1.0 0.2 0.9 1.3 2.8 7.1

Diamond stingray (Dasyatis sp) 18.9 25.5 19.6 24.5 24.6 36.9 150.0

Shovelnose guitarﬁsh (Rhinobatos spp. and Zapteryx spp.) 104.5 139.2 123.9 104.2 109.0 117.5 698.3

TOTAL Batoids 124.2 165.8 143.6 129.7 134.9 157.2 855.4

Angel shark (Squatina californica) 36.8 17.2 48.3 34.9 24.0 34.0 195.1

Small sharks (different species) 11.3 7.0 12.6 4.8 11.2 8.4 55.3

Smooth-hounds (Mustelus spp.) 0 0 0 0 1.0 0.6 1.6

TOTAL Sharks 48.1 24.1 60.9 39.7 36.1 43.0 251.9

TOTAL 296.1 317.6 292.2 247.3 246.4 324.8 1,724.5

were conducted (June 2011–May 2012). The Landings of SDS and and YOY white sharks were consistently caught within BSV during

the number of white sharks caught per month were highest during all years, which fulﬁlls the third criterion (Table 1).

July 2011 and May 2012. SDS landings were high between June and

September and very low during the rest of the year. The number 4. Discussion

of white sharks caught per month and the SDS landings distribu-

tion (Fig. 8a) were not signiﬁcantly different (U = 68.5, n1 = n2 = 12, Our results demonstrate that newborn and YOY white sharks

P = 0.865). are present at BSV every year, and are caught in local ﬁsheries in

The monthly number of white sharks incidentally caught per higher frequencies from May to September. Although JWS are also

tonnes of SDS landings (Fig. 8b), indicated that about one shark present in BSV, they are caught at a lower frequency. Our ﬁndings

was incidentally caught for every tonne of SDS landed during June are clearly consistent with the three criteria proposed by Heupel

through September 2011. During the period from October 2011 to et al. (2007) for the accurate identiﬁcation of shark nursery areas.

February 2012, between one and ﬁve sharks were caught per landed BSV therefore serves as a nursery area for white sharks within the

tonne of SDS (Fig. 8b). Hence, proportionally more juvenile white NEP, and should require the development of speciﬁc management

sharks were captured per tonne of SDS during the fall and winter and conservation strategies to further minimize young white shark

months than during the spring and summer. bycatch mortality.

4.1. White shark incidental catch

3.3. Evaluation of Bahia Vizcaino as a nursery area Gillnets are usually size selective and used principally to catch

species of speciﬁc size ranges. Selectivity curves for a certain mesh

The newborn and YOY white shark data indicates that the ﬁrst size are typically dome-shaped, with highest catches at interme-

criterion established by Heupel et al. (2007) was met; there were diate sizes. Consequently, the range of sizes caught with a gillnet

signiﬁcant differences in the catches between NBSV and BSV, with can typically be controlled by the careful choice of the mesh size

a very low catch of young sharks outside of BSV (5 at NBSV vs. and ﬁlament strength (He and Pol, 2010). The size composition

296 at BSV) (Fig. 3), although similar ﬁshing gear are used in both of juvenile white sharks caught within BSV showed two modes:

areas and along the Baja California coast (Cartamil et al., 2011). one for the 135–140 cm TL size class and a higher one for sharks

The NBSV area had a higher proportion of juveniles (75% of total), 170–175 cm TL. Cartamil et al. (2011) reported that in BSV demer-

while the BSV area had a higher abundance of newborns and YOYs sal teleosts and coastal elasmobranchs (mainly batoids and small

(89%). While newborns and YOYs were caught during most months, sharks) were targeted using bottom-set gillnets deployed on the

the majority of the catches occurred between May and September continental shelf. These nets are made with monoﬁlament and have

(Fig. 5). These results support the second criterion. Finally, newborn lengths of 100–500 m, heights of up to 5.5 m and a stretch-mesh

132 E.C. O˜nate-González et al. / Fisheries Research 188 (2017) 125–137

Fig. 7. Monthly total landings of select demersal species (SDS): a) flounders, b) batoids and c) sharks reported at the fishing offices of Jesus Maria and Guerrero Negro from

2008 to 2013.

sizes of 6–12 cm. Multiple gillnets, either strung together or set in ing, even within the 135–140 cm TL size range (Fig. 3), it is likely

various locations, are often deployed by a single ﬁshing vessel for a that most sharks are caught primarily by entanglement of jaws and

24 h period before retrieval. The maximum number of gillnets used ﬁns.

simultaneously by one vessel is eight (Cartamil et al., 2011). The The high frequency of 170–175 cm TL white sharks is, therefore,

higher proportion of larger YOYs caught within BSV could be asso- likely to be due to the higher abundance of the larger size class

ciated with the selectivity of the ﬁshing bottom gillnets used in the within the bay. Southward movements of juvenile white sharks

area, the higher absolute abundance of individuals within this size from the SCB to the BSV area have been reported based on satellite-

class, or natural mortality of newborns and small YOYs potentially tagged individuals (Weng et al., 2007, 2012). Weng et al. (2007)

being high annually. reported that one 156 cm TL YOY tagged in the SCB September 2003

When gillnets are used, individuals are entangled by gilling (i.e., reached BSV during mid-October of the same year. Three of the

ensnared behind the gill-cover) or by wedging (held by the mesh white sharks tagged by Weng et al. (2012) in the SCB also moved

around their maximum body girth) (Fonseca et al., 2005). However, south, with one white shark (176 cm TL at tagging) entering the

other technical characteristics related to gillnet construction (mesh Gulf of California in mid-June 2008. Another white shark (187 cm

depth/hanging ratio) and twine speciﬁcations (material, thickness, TL) tagged in January 2007 moved along the shore of BSV, and a

color, pound test, etc.) must be considered with the catch size third white shark (166 cm TL) tagged in November 2009 moved to

frequency distribution (Fonseca et al., 2005; He and Pol, 2010). Sim- the BSV close to the mouth of Laguna Ojo de Liebre and was caught

ilarly, anatomical characteristics inﬂuence capture as a function of incidentally in February 2010. All three of these white sharks were

∼

size. Some species are caught via snagging, and high swimming 170–175 cm TL when ﬁrst captured, providing evidence that this

activity or struggling can result in entanglement of body projec- size class has a tendency to migrate toward the waters of BSV.

tions (Fonseca et al., 2005). Given that the mesh size of the gillnets Larger sized white sharks (>175 cm TL) may be able to break free

used in BSV seems to be too small to catch white sharks by wedg- of the nets; local ﬁshermen have commented on the presence of

E.C. O˜nate-González et al. / Fisheries Research 188 (2017) 125–137 133

Fig. 8. Monthly a) Select Demersal Species (SDS) landings in tonnes and number white shark incidental caught, and b) rate of number white sharks (WS) caught as a function

of SDS landings from Jesus Maria and Guerrero Negro between June 2011 and May 2012.

large holes in their nets, which they believe to be caused by sharks during the autumn and winter months, even though SDS landings

escaping capture (E. García-Rodríguez, pers. comm.). Thus, it is pos- decreased substantially, the incidental catches increased to around

sible that larger juvenile and subadult white sharks are interacting four sharks per ton of SDS product landed. Although these results

with bottom gillnets, but they tear the nets and are, therefore, not may be due to changes in relative white shark abundance within

landed. It is also possible that those sharks emigrate out of the area the bay (i.e., higher abundance during autumn or winter), the role

to Guadalupe Island (Hoyos-Padilla et al., 2016) or southern Califor- of changes in the patterns of habitat use over small spatial scales

nia. This would lead to an underestimate in the relative abundance or changes in bottom set gillnet practices have yet to be evaluated.

of sharks greater than175 mm TL. To fully understand the pattern of white shark resource use of

Analysis of SDS landings reﬂect the yearly usage pattern of bot- BSV, annual monitoring of white shark movements, catch rates

tom gillnets in BSV and hence the susceptibility of white sharks and SDS ﬁshery dynamics are necessary. Further, understanding

to local ﬁshing. Cartamil et al. (2011) reported that trap ﬁsheries incidental catch rates within BSV and developing strategies for

targeting spiny lobster (Panulirus interruptus) were the dominant its reduction requires catch-speciﬁc information (e.g., geographic

activity in some ﬁshing camps of BSV during their legal season (15 location inside the bay) and habitat characteristics (e.g., temper-

September–15 February). Some ﬁshermen change to longline ﬁsh- ature, type of bottom, depth). When coupled with movement

ing gear from September to November and February to March (O. studies, certain areas could be identiﬁed as potential conservation

Santana-Morales, pers comm), but white sharks are caught less fre- zones in which ﬁshing activities with speciﬁc gear types (i.e., bot-

quently by longlines than bottom gillnets (Santana-Morales et al., tom set nets) ought to be limited, or the soak time reduced to allow

2012). During the summer months, when the highest landings of for the possibility of live releases (Lyons et al., 2013), or the use of

the SDS were observed, the largest records of incidental juvenile ﬁner ﬁlament size gillnet implemented to allow JWS to break the

white shark catches were also recorded, with approximately one nets and escape.

white shark captured per tonne of landed product. In contrast,

134 E.C. O˜nate-González et al. / Fisheries Research 188 (2017) 125–137

The BSV ﬁshing grounds produces the largest amount of ﬂoun- The third criterion proposed by Heupel et al. (2007) indicates

der and batoid catch for the western coast of Baja California that the seasonal use of the nursery area should be consistent on an

(Table 2). In the case of the ﬂounder group, the primary species annual basis, and our data also met that criterion. In BSV this pattern

landed is the California halibut (Paralichthys californicus), which was ﬁrst observed by Santana-Morales et al. (2012) who reported

ranges from central California to northern Baja California (Allen, the highest incidental catches during June and July between 1999

1988). Juvenile California halibut use coastal lagoons, bays, and and 2010. Our intensive surveys conducted between June 2011

estuaries as nurseries (López-Rasgado and Herzka, 2009), and and May 2012 showed a similar seasonality. Records of inciden-

Laguna Ojo de Liebre has been described as an important habitat for tal catches of white sharks in the SCB showed a similar seasonality,

this lucrative ﬁshery resource (De la Cruz-Agüero et al., 1996). In the with higher frequencies between May and July (Klimley 1985).

case of the batoid group, the main species landed are the shovelnose Conceptually, nursery areas should provide young individuals

guitarfish (Rhinobatos productus) and banded guitarfish (Zapterix with sufficient food resources, favorable growth conditions, and

exasperata) (Cartamil et al., 2011), which range from central Cali- some protection from predators (Beck et al., 2001). BSV has been

fornia to the Gulf of California (Ebert, 2003). YOY and juvenile white characterized as an area with very high productivity within the NEP

sharks have been found to feed on demersal ﬁshes, elasmobranchs that results in a high relative abundance of consumers (Lluch-Belda,

and invertebrates (Klimley, 1985; Dewar et al., 2004). Weng et al. 2000), which could contribute to the diet of naïve neonatal white

(2007) described that 63% of the tagged YOY sharks of their study sharks. Juvenile white sharks in BSV feed on benthic species such

showed a benthic foraging behavior, typically in soft sea bottom as rays (Myliobatis californica, Raja spp.) and crustaceans as well as

areas such as that found in BSV. In the SCB they feed on benthic small pelagics such as bony ﬁshes (Scomber japonicus, Atractosion

prey such as California halibut, round stingrays, and bat rays (C. nobilis) and squid (Teuthoidea) (Santana-Morales et al., 2012). As

Lowe et al., unpubl. data). Therefore, it is likely that juvenile white white sharks grow, they target larger prey, including more pelagic

sharks are caught incidentally in the gillnet ﬁshery while foraging bony ﬁshes (Thunnus spp.), squid (Dosidicus gigas) and other elas-

for demersal prey. mobranchs. Immature white sharks also feed opportunistically on

dead marine mammals (Dicken, 2008). The main prey species of

juvenile white sharks (mostly newborns and YOYs) are benthic

4.2. Bahia Vizcaino as nursery area ﬁshes, which comprise many of the major component of the BSV

ﬁsheries (Cartamil et al., 2011; Santana-Morales et al., 2012). In this

Klimley (1985) used the data on size distribution and seasonal- study, we were able to report on the landings of the BSV bottom

ity of catch records to describe the habitat use of white sharks in gillnet ﬁsheries (Table 2), and show that several of the dominant

the NEP during all life history stages. Given the occurrence of YOY taxa have been reported as important prey items for white sharks

in the region, he suggested that the SCB was a pupping and nursery (Santana-Morales et al., 2012). Most of these species are ﬁshed close

ground for white sharks during the summer months. For adults, he to shore by the artisanal ﬁsheries of BSV (Guerrero-Ávila et al.,

concluded that their primary habitat was central and northern Cali- 2013). Because of the high incidence of capture of white sharks

fornia. Recently, the white shark nursery area has been suggested to proximal to the mouth of lagoons (Guerrero-Ávila et al., 2013), it

include BSV in Baja California (Weng et al., 2007; Domeier, 2012) may be that young white sharks prey upon the same assemblages

based on juvenile shark (>165 cm TL) tagging results and on the that are targeted by ﬁshers of the region.

high frequency of incidentally caught white sharks recorded in the The identiﬁcation of white shark nursery areas in other geo-

local ﬁsheries (Weng et al., 2007; Santana-Morales et al., 2012). Our graphic regions throughout their distribution has been conducted

study formally assessed BSVıs´ function as a nursery habitat using a largely based on tagging studies. Some habitats in eastern Australia

robust conceptual framework and the speciﬁc criteria proposed by have been proposed as nursery areas for white sharks, including

Heupel et al. (2007). Cornet Inlet and the Port Stephen estuarine system (Bruce and

The ﬁrst criterion proposed by Heupel et al. (2007) stipulated Bradford, 2012). Cornet Inlet is similar to BSV in that is a productive

that a shark nursery area should exhibit the presence of immature habitat that supports several immature white sharks prey species,

sharks in greater abundances than in other areas. Our results indi- such as stingrays (Dasyatis brevicaudata), perch (Johnius belangerii),

cate that BSV had a much higher incidental catch rate of newborn and ﬂathead (Platycephalus endrachtensis) (Barton et al., 2012). The

and YOY sharks compared to any location along the northern Baja Port Stephen estuarine system is also similar to BSV and Cornet Inlet

California peninsula. The high frequency of catches of these early- in that it is also extremely productive and rich in potential prey

stage white sharks within the BSV region parallels that of similar (Oke and Middleton, 2001), with a high abundance of ﬁsh species

nursery “hotspots” in the SCB, which have also been proposed to such as Australian salmon (Arripis trutta), Australasian snapper

serve as nursery habitats (Lowe et al., 2012; Lyons et al., 2013), (Pagrus auratus), mulloway (Argyrosomus hololepidotus), striped

although these observations have not been formally tested against mullet (Mugil cephalus), and gummy shark (Mustelus antarcticus), as

the Heupel et al. (2007) criteria. well as various other elasmobranchs (e.g., eagle rays Myliobatis aus-

With regards to the second criterion, Heupel et al. (2007) tralis), all of which are common prey for JWS (Bruce and Bradford,

established the need for seasonality in the presence of newborns 2012). Dicken and Booth (2013) examined data from aerial sight-

and YOY sharks. Our results suggest that YOY white sharks were ings and shore based angling and found that YOY and JWS are

caught mostly between May and September, while newborns were present during the spring and summer months in certain sites

recorded in high numbers during June and July, and this was seen within Algoa Bay, South Africa. Their data only supported the ﬁrst

during all years analyzed. June and July coincides with the season and third criteria proposed by Heupel et al. (2007), and they, there-

when adult females (supposedly pregnant) tagged at Guadalupe fore, refrained from designating the region as a nursery area. The

Island return from their offshore migrations to the nearshore white shark nursery areas that have been identiﬁed to date (i.e.

waters close to BSV as well as the inside the Gulf of California SCB, BSV, Cornet Inlet, Port Stephen, New York Bight, and the Sicil-

(Domeier and Nasby-Lucas, 2013). It has been suggested that the ian Channel; Casey and Pratt, 1985; Bruce and Bradford, 2012) are

parturition area for these Guadalupe Island sharks may be close to similar in that they have a broad continental shelf and harbor the

shore in the middle part of the Baja peninsula and potentially in an presence of abundant potential prey for newborn and YOY white

area around the central west coast of Gulf of California (Domeier sharks. Further analysis related with habitat characteristics in rela-

and Nasby-Lucas, 2013). Hence, our data clearly support a seasonal tion to refuge and oceanographic conditions are still pending.

pattern in the presence of young life stages in the BSV.

E.C. O˜nate-González et al. / Fisheries Research 188 (2017) 125–137 135

Werry et al. (2012) suggested that there was a white shark for 1999–2013. However, when we analyzed the incidental catch

migration corridor between the “hot spots” Cornet Inlet and the records during the intensive sampling effort carried out between

Port Stephen estuarine system; Bruce and Bradford (2012) sug- May 2011 and May 2012, an estimate of 175 white sharks per year

gested these coastal areas should be considered as nursery areas. was obtained. Although a misidentiﬁcation of some of the ﬁsher-

The high frequency of observations of YOYs in the SCB and BSV also men records we include in our data set is possible, it is important to

suggests that these two areas may be regional “hot spots” of high consider that the relatively high estimate of 175 white sharks per

abundance for this age class. Previous tagging studies indicate that year corresponds to the period before the implementation of the

there might be a migration corridor between the two areas, espe- seasonal summer closure. To evaluate the effect of this seasonal clo-

cially for sharks larger than 165 cm TL (Weng et al., 2007, 2012). sure, we focused solely on the records from June to December 2012

The results of Bruce and Bradford (2012), Werry et al. (2012) and and obtained an annual estimate of approximately 91 white sharks

those presented here suggest that pregnant female white sharks caught per year (corresponding to a 52% decrease in the incidental

may seek regions of high prey abundance for parturition. Repre- catch). These results, coupled with the landing records, suggest a

sentative sampling of the area between the SCB and BSV, as well positive effect of the seasonal closure on the immature white shark

as tracking studies of young white sharks in BSV, are necessary to population. A recent white shark population estimate for the NEP

determine whether the region between SCB and BSV is in fact a con- indicated ∼3000 white sharks in the region (Dewar et al., 2013;

sistent migration corridor for young sharks, and whether foraging Burgess et al., 2014), although there is limited information regard-

takes place during these geographical movements. In summary, the ing the species’ population dynamics in the NEP. The magnitude

data are consistent with the Heupel et al. (2007) criteria, and BSV of the annual incidental catch of young white sharks in Mexican

can, therefore, be considered as a white shark nursery area. waters (between 25 and 175 individuals per year depending on the

period examined) could have a substantial negative impact on the

4.3. Management implications larger white shark population in the NEP.

Understanding the patterns of nursery habitat use is impor-

The year-round presence of white sharks in BSV coupled with tant for the management and conservation of white sharks in the

the high incidental capture of young individuals supports the press- NEP. The Mexican government has established the white shark as a

ing need to enforce current regulations within this region. Since threatened species (DOF, 2002), and it has initiated a ﬁshing ban for

2012, an elasmobranch ﬁshing closure has been established from this species in Mexican waters and white sharks must be released

May to July (DOF, 2012) along the entire Mexican Paciﬁc Coast. when captured (DOF, 2014). The mandatory release of live sharks

Although the protection of white sharks is not the speciﬁc purpose may provide an additional means of reducing ﬁshing mortality,

of this regulation, the timing of this ﬁshery closure does coincide especially within BSV. Given the high survivorship of post-release

with time of year when immature sharks are found close to shore. net captured sharks in the SCB (Lyons et al., 2013), the implemen-

The temporal change in the catch patterns reported in this study tation of other ﬁshing protocols, such as decreasing the soak time

st st

(Fig. 7), likely reflects the beginning of the May 1 –July 31 elas- or use finer filament size, could be implemented to further reduce

mobranch ﬁsheries closure. These data indicate that during 2012 incidental mortality. When coupled with the existing management

the ban was not effective until July, and for 2013 it was effec- and conservation measures, such speciﬁc addition changes could

tive only between May and June. These results suggest the need make a signiﬁcant contribution towards conserving the juvenile

to strengthen surveillance in the implementation of the closures. white sharks in the NEP.

Improved education and enforcement of this management mea-

sure should contribute to the survival of young white sharks by Acknowledgements

decreasing the incidental catch.

Our results indicate there is high incidental ﬁshing pressure on We gratefully acknowledge the ﬁsheries communities from

juvenile white sharks within Mexican waters compared with the Popotla, Eréndira, Camalú and Laguna Manuela in BC, and Las

incidental catch records at SCB (Lowe et al., 2012; Lyons et al., Casitas in BCS (especially Edgar Zepeda) for their assistance and

2013). This has implications for the overall status of the white help with ﬁeldwork and loobooks data. This work was supported by

shark population in the NEP. Mollet and Cailliet (2002) assessed Monterey Bay Aquarium-MBA (awarded to OSN), The Rufford Small

the importance of immature stages of several species, including Grant Foundation-RSGF foundation grant no. 10774 (awarded to

the white shark, by comparing different demographic models (i.e., ECOG). The ﬁrst author received a graduate fellowship from CONA-

life history tables, Leslie matrices and stage-based matrices) and CYT to support his PhD program in Marine Ecology at CICESE. This

incorporating survival and population growth rates of newborns, paper is dedicated to the memory of Miguel Ángel Escobedo Olvera

juveniles and adults. Stage-based models better explained popula- “Micks”.

tion trends in a slow-growing species such as the white shark, and

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