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176
J. Black Sea/Mediterranean Environment
Vol. 26, No. 2: 176-189 (2020)
RESEARCH ARTICLE
Exploring a possible nursery ground of white shark
(Carcharodon carcharias) in Edremit Bay (northeastern
Aegean Sea, Turkey)
Hakan Kabasakal
ORCID ID: 0000-0001-8189-9748
Ichthyological Research Society, Tantavi Mah., Menteşoğlu Cad., İdil apt., 30/4, 34764
Ümraniye, İstanbul, TURKEY
Corresponding author: kabasakal.hakan@gmail.com
Abstract
Between 1 July 2008 and 14 April 2018, five young-of-the-year (YOY) (TL range 85-175
cm) and six juvenile (TL range 180-300 cm) white sharks (Carcharodon carcharias) were
caught off the Turkish coast of the Aegean Sea. The mean length + standard deviation of
YOY and juvenile white sharks were 138.1+34 cm and 206.6+46 cm, respectively. The
YOY white sharks were caught only in Edremit Bay and juveniles were captured in several
localities outside of the mentioned region. Based on the findings of previous studies, it is
suggested that Edremit Bay may serve as a nursery ground for C. carcharias in the northern
Aegean Sea and the surrounding insular marine area outside of the bay waters, may serve
as a growing and feeding ground for juveniles until maturity. The white shark population
in the Mediterranean may be considered at greater risk of local extirpations than previously
thought, and effective management of Edremit Bay as a nursery ground is crucial regarding
the overall survival of white sharks in the Mediterranean.
Keywords: Nursery ground, white shark, Carcharodon carcharias, Aegean, conservation,
survival
Received: 25.05.2020, Accepted: 14.08.2020
Introduction
Nursery areas, which have been recognized as a concept in the scientific literature
for nearly a century, are widely considered to be essential habitats for sharks
(Heithaus 2007; Heupel et al. 2007). Since shark nurseries have been defined as
essential habitats for breeding of a given shark species (Heithaus 2007), the
development of appropriate management for nursery areas relies on the ability to
177
accurately identify those areas that are of greatest importance (Heupel et al.
2007).
White shark, Carcharodon carcharias (Linnaeus, 1758), is one of the four species
of the family Lamnidae, occurring in the Mediterranean Sea. It is an epipelagic
shark, inhabiting coastal and off shore waters, from surface down to a depth of
1300 m (Serena 2005). Its distribution range includes the whole Mediterranean,
but currently absent in the Marmara and Black Seas (De Maddalena and Heim
2012; Kabasakal 2014). Global distribution of C. carcharias extends in temperate
oceans of both hemispheres, and rarely found in tropical waters (Serena 2005).
White sharks can be defined as ‘nomads’ of the oceans, because of their two-year
long-distance migrations between widely separated nursery areas (Domeier and
Nasby-Lucas 2013). Male and female white sharks are known to have site fidelity,
which is termed as ‘philopatry’ (Domeier and Nasby-Lucas 2013; Gubili et al.
2010), which means that adults will return to the areas for breeding, where they
were born.
In the recent Red List assessment by Rigby et al. (2019), global conservation
status of C. carcharias was evaluated as vulnerable; however, according to Dulvy
et al. (2016) and Otero et al. (2019), C. carcharias is critically endangered in the
Mediterranean Sea. Therefore, effective management of its nursery grounds is
crucial for the survival of the species in the Mediterranean, where it has little or
no contemporary immigration from the Atlantic (Gubili et al. 2010). Due to the
occurrence of young-of-the-year (YOY) and pregnant female white sharks,
Tunisian and Sicilian neritic waters have been historically and contemporarily
considered as the main nursery area of C. carcharias in the Mediterranean Sea
(Boldrocchi et al. 2017; Bradai et al. 2012; De Maddalena and Heim 2012;
Fergusson 1996; Saidi et al. 2005). According to Boldrocchi et al. (2017),
between the second half of the 19th and the begining of the 20th century, Sibenik
Bay and the nearby Kvarner Gulf area might also serve as a nursery ground for
C. carcharias.
Following the incidental captures of two newborn specimens in Edremit Bay
(Figure 1), in early July 2008 (Kabasakal and Gedikoğlu 2008), three more YOY
white sharks were also incidentally captured in the same area (Kabasakal 2014;
Kabasakal et al. 2018). Occurrence of five YOY specimens in a close vicinity in
different years suggests that Edremit Bay may serve as a nursery area for C.
carcharias in the northern Aegean Sea. Since appropriate management of nursery
areas relies on accurate identification and mapping of these essential habitats
(Heupel et al. 2007), it is crucial to determine the approximate boundaries of this
possible nursery ground in Edremit Bay. In the present study, based on available
data, attempts to draw a preliminary map of this nursery ground are made, and
the implications of commercial fisheries, continuing in the same region are
discussed.
178
Materials and Methods
Study Area
The Aegean Sea is topographically divided into two basins by (approximately)
the 38° parallel, i.e. into the north and south Aegean (Papaconstantinou 1992).
Mean monthly sea surface temparatures vary from 8°C in the north during winter,
up to 26°C in the south during summer (Poulos et al. 1997). The Aegean
archipelago is a typical archipelago of continental islands, which are forming
groups of minor islands in wide marine space (Türküstün 2015).
Figure 1. Map showing the capture localities of YOY and juvenile white sharks, off
Turkish coast of Aegean Sea. Numbers are same with those in Table 1.
179
Data Collection
Since the white shark is a critically endangered species and protected in certain
parts of the Mediterranean (Otero et al. 2019; Serena 2005), the selection of an
appropriate sampling method for the present study was an instance of typical
opportunistic research, consisting in dead animal sampling (Jessup 2003). A
regular screening of scientific literature, social media, local newspaper - both
printed and online - provided information on the YOY and juvenile white sharks,
incidentally captured off Turkish coast of Aegean Sea (Figure 1). Nine out of 11
white sharks were previously published and relevant information of these
specimens were exctracted from Kabasakal (2014), Kabasakal and Gedikoğlu
(2008), Kabasakal and Kabasakal (2015), and Kabasakal et al. (2009, 2018). Two
specimens are new records (Table 1). Capture data (type of fishing gears, date
and locality of captures, total length (TL) in cm and weight (W) in kg) were
recorded for new specimens. Age distribution of YOY and juvenile white sharks
was assessed using the following length categories (Boldrocchi et al. 2017): YOY
(<1.75 m TL) and juvenile (>1.75-3.0 m TL).
Results and Discussion
Between 1 July 2008 and 14 April 2018, five YOY (TL 85-175 cm) and six
juvenile (TL 180-300 cm) white sharks were caught off Turkish coast of Aegean
Sea (Figure 1). These specimens are depicted on Figures 2 and 3, and relevant
information are presented in Table 1. The mean length + standard deviation of
YOY and juvenile white sharks were 138.1+34 cm and 206.6+46 cm,
respectively. YOY white sharks (specimens 1, 2, 5, 7 and 9) were caught only in
Edremit Bay and juveniles were captured in several localities outside of the bay
(Gökçeada, specimens 3 and 8; Çanakkale, specimen 4; Yeni Foça, specimen 6;
Karaburun, specimen 11; and Didim, specimen 10; Table 1; Figure 1). One of the
YOY white sharks (specimen 5) was released alive (Figure 3). Two specimens
(18.1%) were captured in purse-seining fishery, and eight specimens (72.7%)
were incidentally captured by artisanal fishermen deploying coastal stationary-,
gill- or trammel-nets, and one specimen (9.09%) was captured by means of a
bottom-trawler. Thus, nearly 82 % (n=9) of the YOY and juvenile white sharks
were captured in demersal fisheries.
Umbilical scars were seen in three newborns (specimens 1, 2 and 5; Figure 4),
which were captured in early July (Table 1), and other two YOY white sharks
were captured in January and April. Juvenile white sharks were captured in April
(n=2), June (n=1), September (n=1), January (n=1) and February (n=1) (Table 1).
Most of the young white sharks were recorded in spring and summer months.
180
Figure 2. YOY and juvenile white sharks examined in the present study. (A) specimen 7;
(B) specimen 4; (C) specimen 6; (D) specimen 10; (E) specimen 9; (F) specimen 8;
(G) specimen 11; (H) specimen 1; (I) specimen 3; and (J) specimen 2. Specimen
numbers are same with the numbers accompanying the bold dots (●) seen on Figure 1.
Capture details of the specimens are presented on Table 1.
Figure 3. Captured images from the video of releasing a YOY white shark
(specimen 5 in Table 1, Figure 1), off the coast of Altınoluk
(Video footage: Cenk Balkan).
181
Table 1. Capture data and relevant references of YOY and juvenile white sharks
examined in the present study
No*
Date
Locality
TL
(cm)
W
(kg)
Gear
References
1
1 July 2008
Altınoluk
125,5
-
Gill-net
Kabasakal and Gedikoğlu
(2008)
2
4 July 2008
Altınoluk
145
-
Gill-net
Kabasakal and Gedikoğlu
(2008)
3
21 Feb. 2009
Gökçeada
180
47.5
Bottom-trawl
Kabasakal et al. (2009)
4
15 April 2009
Çanakkale
300
102
Purse-seine
Kabasakal et al. (2009)
5
6 July 2011
Altınoluk
85
-
Trammel-net
Kabasakal (2014)
6
19 Sept. 2014
Yeni Foça
200
40
Stationary-
net
Kabasakal and Kabasakal
(2015)
7
2 January 2016
Altınoluk
175
-
Stationary-
net
Kabasakal et al. (2018)
8
January 2017
Gökçeada
180
-
Stationary-
net
This study
9
April 2017
Altınoluk
160
-
Gill-net
This study
10
4 June 2017
Didim
200
60
Purse-seiner
Kabasakal et al. (2018)
11
14 April 2018
Karaburun
180
-
Stationary-
net
Kabasakal et al. (2018)
*Numbers seen in ‘No’ column are same with the numbers in Figure 1.
In a recent study on distribution, ecology and status of the white shark in the
Mediterranean Sea, Boldrocchi et al. (2017) reported on the captures of 29 YOYs
in several locations, including the Aegean Sea where six out of 29 Mediterranean
YOYs were captured. Furthermore, Boldrocchi et al. (2017) stated that juvenile
white sharks have been recorded in all regions of the Mediterranean, except in the
Marmara Sea. Available data on the occurrence of C. carcharias in Turkish
waters reveal that YOY or juvenile white sharks have not been historically or
contemporarily occurred in the Marmara Sea (Kabasakal 2003, 2014).
Movements of white sharks in the Mediterranean Sea is closely associated with
the migrations of the bluefin tuna, Thunnus thynnus (Linnaeus, 1758) (De
Maddalena and Heim 2012). Majority of the historical catch records of C.
carcharias in the Marmara Sea consisted of adult specimens (>450 cm TL),
which have been the bycatch of tuna handliners (Kabasakal 2003, 2016).
Presently it can only be speculated that the Marmara Sea might have served as a
historical feeding ground for adult white sharks. The mean length of YOYs
recorded in several parts of the Mediterranean Sea ranged from 104+24.9 cm
(Aegean Sea) to 151+14.1 cm (Sicilian Channel) (Boldrocchi et al. 2017). With
the addition of recent captures of specimens with TL 160 and 175 cm (specimens
7 and 9), however, mean TL of YOYs in the Aegean Sea should be updated as
138.1+34 cm.
182
Figure 4. Umbilical scars (birth marks) on the ventral surfaces of neonates; (A)
specimen 1, and (B) specimen 2 in Table 1.
The seasonality of occurrence of YOYs and juveniles in the Turkish Aegean Sea
well coincides with the seasonality data presented by Boldrocchi et al. (2017),
Santana-Morales et al. (2012), De Maddalena and Heim (2012), and White et al.
(2019), who reported a close affinity of the high numbers of occurrences with the
warmer months of the year. According to Boldrocchi et al. (2017) and De
Maddalane and Heim (2012), YOYs were captured in spring and summer months
in the Mediterranean. In the present study, four out of five YOYs were captured
in summer (early July, specimens 1, 2 and 5) and mid-spring (April, specimen 9),
and one YOY was captured in winter (January, specimen 7) (Table 1). Total
length of the specimen 7 YOY was 175 cm, when it was captured in January, and
at that time no birth mark (umbilical scar) was seen. Thus, it can be supposed that,
183
the specimen 7 was born in the preceeding summer, and remained in Edremit Bay
nursery ground for further growing. According to Santana-Morales et al. (2012),
the umbilical scar was still visible in the white shark specimens of 150 and 163
cm TL.
Although juvenile white sharks are known to frequent inshore water (Harasti et
al. 2017), they are also known to travel for relatively long distances beyond the
perimeters of their nurseries (see eg. Bruce et al. 2019; Weng et al. 2007). Weng
et al. (2007) reported on a YOY, which moved 700 km away from its nursery
between late September and mid October. In a recent survey dealing with the
broad-scale movements of juvenile white sharks in eastern Australia, Bruce et al.
(2019) found that juveniles can travel for 1800 km, crossing from Bass Strait to
New Zealand. Soutward and northward occurrences of juveniles in remote
regions outside of Edremit Bay nursery were also observed (Figure 1). In the
northward of Edremit Bay, three juveniles were captured off Çanakkale and
Gökçeada coasts (specimens 3, 4 and 8), and in the southward, two juveniles
(specimens 6 and 11) were captured off İzmir coast, and one juvenile (specimen
10) was captured off Didim coast. As it is clearly seen on Figure 1, Aegean
seabord of Turkey has a peninsular coastline and assuming that specimen 11 was
born in Edremit Bay, then it should have been travelled more than 500 km before
it was captured off Didim. For the moment, on the basis of available data, it is not
possible to answer the question, whether specimen 11 was born in Edremit Bay
or in another unidentified nursery in the southern Aegean Sea. Despite the
uncertainties about the provenance of specimen 11, it had enough potential for
travelling from Edremit Bay to Didim, as suggested by the movement data of
juveniles given by Bruce et al. (2019) and Weng et al. (2007).
Offshore and coastal islands appear to offer several advantages to YOYs and
juveniles, as revealed, for example, by the studies of Curtis et al. (2018), Hoyos-
Padilla et al. (2016) and Klimley (1985). The preference for coastal and insular
water of the YOY and juvenile white sharks is reflected by the relatively shallow
depths at which these sharks were captured in the present study. Depth of the
bottom where the juvenile white sharks were captured was less than 150 m and
YOYs were captured in water as shallow as 10 m. As suggested by Hoyos-Padilla
et al. (2016), insular marine areas provides juvenile white sharks with an
opportunity to start their first offshore migrations, probably for feeding on
demersal prey and then coming back to their nursery grounds to avoid predators.
From this perspective, Edremit Bay nursery ground, which is surrounded by
offshore and coastal islands, provides a habitat for growing juveniles to gain
experience of movement between offshore islands and nearshore before departing
for long-distance migrations. Hoyos-Padilla et al. (2016) found that tagged
juvenile white sharks remained near Guadalupe Island for 12 to 14 months before
departing distant regions.
184
Throughout its global distribution range, survival of young white sharks is
threatened by the pressure of coastal artisanal fisheries with stationary nets, such
as gill-net or trammel-net fishery (Klimley 1985; Santana-Morales et al. 2012).
According to Santana-Morales et al. (2012), highest incidental captures of
juvenile white sharks were recorded in the artisanal bottom-set gill-nets, with
nearly 75% of sharks caught using this fishing gear in western Baja California
(Mexico). Curtis et al. (2018) also stated that bycatch of juvenile and YOY white
sharks in the New York Bight (western north Atlantic) occurs in gill-net fishery.
In an extensive research on the interactions of juvenile white sharks with gill-net
fishery, Lyons et al. (2013) reported that gill-net fishery is significantly and
positively correlated with the incidence of white shark captures. In the present
study, nearly 73% (8 out of 11) of white sharks were incidentally captured by
bottom-set nets, including stationary- (36.3%), gill- (27.2%) and trammel-nets
(9.09%). The addition of one specimen (9.09%), which was captured by a bottom-
trawler, reveals that nearly 82% (9 out of 11) of juveniles and YOYs of the present
study were captured in demersal fisheries (Table 1).
Previous studies revealed that, juvenile white sharks feed primarily on bottom
dwelling fishes (White et al. 2019), and nursery grounds in their coastal habitats
may overlap with areas highly impacted by fisheries (Boldrocchi et al. 2017).
According to Domeier and Nasby-Lucas (2013), YOY and juvenile white sharks
do not have the mass and strength for breaking through most commercial fishing
gear, thus they represent the most vulnerable stage of C. carcharias.
In conclusion, based on incidental captures of YOY white sharks between 2008
and 2018, it is suggested that Edremit Bay may serve as a nursery ground for C.
carcharias, in the northern Aegean Sea, and the surrounding insular marine area
from northward to southward outside of bay waters, may serve as a growing and
feeding ground for juveniles until maturity. Since juvenile fish abundance in
nursery areas, including YOYs, may provide an estimate of recruitment trends
(Harasti et al. 2016), an extensive in situ survey with nondestructive methods is
required to investigate the habitat use, site fidelity, relative abundance, seasonal
occurence and movements of YOY and juvenile white sharks, occurred in the
Edremit Bay and surrounding marine area. Since the white shark is critically
endangered in the Mediterranean Sea (Otero et al. 2019), the use of stereo-
BRUVs (Baited Remote Underwater Video) may provide a viable and
nondestructive method to obtain estimates of the size and presence of white
sharks, as proposed by Harasti et al. (2016). Based on available genetic data
(Gubili et al. 2010), Mediterranean white shark population may be considered at
greater risk of local extirpations than previously thought, and effective
management of Edremit Bay as a possible nursery ground is crucial regarding the
overall survival of Mediterranean white sharks.
185
Acknowledgments
Author thanks to fishermen for their friendly contributions during the white shark
investigation in Turkish waters which has been continuing since 2003. A special thank
goes to Mr. Cenk Balkan, for generously sharing the video of specimen 5. Author also
thanks to anonymous referees for their comments.
Edremit Körfezi’nde (kuzeydoğu Ege Denizi) büyük
beyaz köpekbalığının (Carcharodon carcharias) olası
üreme alanı
Öz
1 Temmuz 2008 ve 14 Nisan 2018 tarihleri arasında, Ege Denizi’nin Türkiye kıyılarında
5 tane yenidoğan (TB aralığı 85-175 cm) ve 6 tane juvenil (TB aralığı 180-300 cm) büyük
beyaz köpekbalığı yakalanmıştır. Yenidoğan ve juvenil büyük beyaz köpekbalıklarının
ortalama tam boyları (TB), sırasıyla, 138.1+34 cm ve 206.6+46 cm’dir. Yenidoğanlar
sadece Edremit Körfezi’nde yakalandıkları halde, juveniller körfez dışında kalan farklı ve
körfeze uzak bölgelerde yakalanmışlardır. Eldeki veriler, Edremit Körfezi’nin kuzey Ege
Denizi’nde C. carcharias’ın üreme alanı olduğunu akla getirmektedir. Ayrıca, körfezin
yakın ve uzak çevresindeki adaları kuşatan deniz alanları, görünüşe göre juvenil büyük
beyaz köpekbalıklarına olgunluğa erişinciye kadar beslenme ve gelişme alanı
sağlamaktadır. Akdeniz’de büyük beyaz köpekbalığı popülasyonunun karşı karşıya olduğu
yok olma riski düşünüldüğünden daha fazla olabilir. Bu bakımdan, Edremit Körfezi’ndeki
üreme alanında etkin bir yönetim planı uygulanması, Akdeniz’de büyük beyaz
köpekbalıklarının genel sağkalımları açısından kritik önemdedir.
Anahtar kelimeler: Üreme alanı, büyük beyaz köpekbalığı, Carcharodon carcharias,
Ege Denizi, koruma, sağkalım
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