This article was downloaded by: [RMIT University]

On: 17 August 2015, At: 07:49

Publisher: Taylor & Francis
Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: 5 Howick
Place, London, SW1P 1WG

African Zoology
Publication details, including instructions for authors and subscription information:
http://www.tandfonline.com/loi/tafz20

Molecular species identification and population

genetics of chondrichthyans in South Africa: current
challenges, priorities and progress
a b
Aletta E Bester-van der Merwe & Katie S Gledhill
a
Molecular Breeding and Biodiversity Group, Department of Genetics, Stellenbosch
University, Stellenbosch, South Africa
b
South African Shark Conservancy, Old Harbour Museum, Hermanus, South Africa
Published online: 11 Aug 2015.

Click for updates

To cite this article: Aletta E Bester-van der Merwe & Katie S Gledhill (2015): Molecular species identification and
population genetics of chondrichthyans in South Africa: current challenges, priorities and progress, African Zoology

To link to this article: http://dx.doi.org/10.1080/15627020.2015.1063408

PLEASE SCROLL DOWN FOR ARTICLE

Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained
in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no
representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of
the Content. Any opinions and views expressed in this publication are the opinions and views of the authors,
and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied
upon and should be independently verified with primary sources of information. Taylor and Francis shall
not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other
liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or
arising out of the use of the Content.

This article may be used for research, teaching, and private study purposes. Any substantial or systematic
reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any
form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://
www.tandfonline.com/page/terms-and-conditions
 African Zoology 2015: 1–13 Copyright © Zoological Society
Printed in South Africa — All rights reserved of Southern Africa
AFRICAN ZOOLOGY
This is the final version of the article that is ISSN 1562-7020 EISSN 2224-073X
published ahead of the print and online issue http://dx.doi.org/10.1080/15627020.2015.1063408

Molecular species identification and population genetics of

chondrichthyans in South Africa: current challenges, priorities and progress
Aletta E Bester-van der Merwe1* and Katie S Gledhill2

1 Molecular Breeding and Biodiversity Group, Department of Genetics, Stellenbosch University, Stellenbosch, South Africa
2 South African Shark Conservancy, Old Harbour Museum, Hermanus, South Africa
* Corresponding author, email: aeb@sun.ac.za

Molecular genetic techniques, such as DNA barcoding and genotyping, are increasingly being used to assist with the
conservation and management of chondrichthyans worldwide. Southern Africa is a shark biodiversity hotspot, with
a large number of endemic species. According to the IUCN Red List, a quarter of South Africa’s chondrichthyans are
threatened with extinction. South Africa’s commercial shark fisheries have increased over the last decade and there
is a need to ensure sustainable utilisation and conservation of this fisheries resource. Here, we give an overview
of the molecular techniques that are used to assist in the identification of species, cryptic speciation and possible
Downloaded by [RMIT University] at 07:49 17 August 2015

interspecific hybridisation, as well as the assessment of population structure and reproductive behaviour of endemic
and commercially important chondrichthyan species of southern Africa. We discuss the potential application of
these techniques for management and conservation of several species affected by South African fisheries. Acquiring
baseline barcode data of all chondrichthyans in southern African waters and assessing the population structure of
exploited species on a local and greater regional scale are recommended as research priorities. Future prospects
should also include high-throughput molecular marker development and investigation of intraspecies functional
variation using next generation sequencing technology.

Keywords: chondrichthyans, conservation, fisheries, genetics, sharks, southern Africa

Introduction

The increasing use of and advances in molecular
techniques have allowed for a more integrated approach
to conservation management of exploited chondrichthyan
species in recent years (Dudgeon et al. 2012). Molecular
tools, including genetic markers and genotype data,
provide the means to assess dispersal abilities, population
connectivity and size, as well as reproductive strategies
within species (Portnoy and Heist 2012). This provides an
insight into the evolutionary and biological processes that
shape species and populations. Advantages of molecular
techniques are numerous and are increasingly applied
to substantiate morphology-based species identification
(reviewed in Hebert et al. 2003) and stock structure
assessments (Ovenden et al. 2015). Molecular genetics
are further used to identify the species composition of
a fishery (Doukakis et al. 2011; Sembiring et al. 2015),
identify which species are being traded, including
threatened species (Chapman et al. 2003; Abercrombie
et al. 2005), and to demonstrate seafood mislabelling or
seafood fraud (Barbuto et al. 2010; Cawthorn et al. 2012).
Genetic population structure within a species can be
assessed on a local, regional or global scale with important
management implications (Keeney et al. 2005; Dudgeon
et al. 2009). With knowledge expanding and technology
costs decreasing, advances and applications in the field
of genetics in southern Africa are now more accessible
to the developing region. In light of the global change
and increased pressure on marine resources, failure to
incorporate genetic information into future management and
conservation of chondrichthyans puts the unique regional
biodiversity and future populations at risk.
Chondrichthyans (sharks, rays and chimaeras) are
a relatively small evolutionarily conservative group of
cartilaginous fishes of ~1 200 species that have been
present in the world’s oceans for at least 400 million
years (Fowler et al. 2005). Globally, there is a growing
concern for shark populations. Approximately 100 million
sharks are harvested annually (Worm et al. 2013),
with commercial fisheries, largely driven by the Asian
shark fin market, contributing to a large proportion of
this decline (Clarke et al. 2006, 2007; Dulvy et al. 2008).
Based on the assessments from the International
Union for the Conservation of Nature (IUCN) Red List
of Threatened species (hereafter referred to as IUCN
Redlist), approximately one-quarter of all chondrichthyans
are threatened with extinction (Dulvy et al. 2014), making
them one of the most vulnerable extant vertebrate groups.
Life-history traits, such as slow growth rates, late age at
maturity, low fecundity and small litter sizes, make it difficult
for many chondrichthyan populations to recover from
anthropogenic pressures (Musick et al. 2000; Stevens et al.
2000; Field et al. 2009).
South-east Africa is recognised as a global shark
biodiversity hotspot (Lucifora et al. 2011). An estimated
30% of species are endemic to South Africa and
neighbouring countries, such as Namibia and Mozambique

African Zoology is co-published by NISC (Pty) Ltd and Taylor & Francis
 2 Bester-van der Merwe and Gledhill
(Compagno 1999). In the latest comprehensive review,
185 species of chondrichthyans were recorded in South
African waters and consist of 109 shark species, 68 ray
species and eight chimaera species (Compagno et al.
2005). Approximately 20 additional species have since
been described, redescribed or newly documented in South
African waters, particularly rays and deep-dwelling species
(e.g. Smale et al. 2002; Ebert and Compagno 2007,
2009; Aschliman et al. 2010; Kemper et al. 2010; Ebert
et al. 2011; Ebert and Cailliet 2011; Ebert et al. 2015).
Despite this large level of biodiversity and endemism,
our knowledge of South African chondrichthyans is
relatively scarce (Compagno 1999; Ebert and van Hees
2015). Furthermore, approximately one-third of the
southern African species are classified as rare and are
known from less than 10 records of each species (RSA
2014). A diverse range of habitats over a small spatial
scale restricts distribution ranges within many species,
resulting in low abundance and pronounced vulnerability
Downloaded by [RMIT University] at 07:49 17 August 2015
to over-fishing (Turpie et al. 2000; Best et al. 2013). There
is evidence of declines for many shark species in South
Africa, based on fishery-dependent and -independent
catch data (Dudley and Simpfendorfer 2006; da Silva and
Bürgener 2007), while it is difficult to determine the impact
that fisheries have on ray and skate species, as there is
a lack of species-specific data (Attwood et al. 2011; Best
et al. 2013). This is particularly concerning, since Dulvy et
al. (2014) identified rays as among the most threatened
of global chondrichthyan taxa. In line with global trends,
approximately one-quarter of chondrichthyan species found
in southern African waters are listed as threatened in the
IUCN Red List (IUCN 2009; Dulvy et al. 2014).
South African shark fisheries have gained a significant
profile over the last decade with increased shark exports
from South Africa expanding into the fintrade and shark
fillet industry (da Silva and Bürgener 2007). To meet the
high demand, a large number of sharks are caught in South
Africa via directed and by-catch fisheries with a total shark
catch estimated at 6 562 t y−1 (DAFF 2013). Approximately
49% of local chondrichthyan species are affected by nine
fisheries in South Africa (da Silva et al. 2015). The main
species that are affected by the demersal shark trade
include smoothhound sharks (Mustelus mustelus Linnaeus,
1758), tope sharks (Galeorhinus galeus Linnaeus, 1758),
bronze whaler sharks (Carcharhinus brachyurus Günther,
1870), dusky sharks (Carcharhinus obscurus Lesueur,
1818) and whitespotted smoothhound sharks (Mustelus
palumbes Smith, 1957) (da Silva and Bürgener 2007).
These, and the other shark species affected by the South
African fisheries (estimated 2010 catch 1 t; DAFF 2013),
are listed in Table 1, together with their respective IUCN
Redlist status. The endemic ploughnose chimaera species,
Callorhinchus capensis Duméril, 1865, is also listed since
the total catch in 2010 was estimated to be approximately
900 t (DAFF 2013).
In this paper, we aim to highlight the important gaps in
genetic information of southern African chondrichthyan
species, with particular reference to issues related to
species identification, taxonomy and cryptic speciation,
population structure and reproductive behaviour. We
provide examples on how molecular genetics can be
used to assist with the management and conservation of
southern African sharks and discuss issues in light of the
unique chondrichthyan biodiversity and fisheries challenges
in terms of species and stock structure identification for a
developing region.
Species identification and related issues for shark
fisheries management
One of the most basic and fundamental, but arguably one
of the most important, requirements for sound conservation
and management is the correct identification of species.
Effective planning and enforcement of management
regulations is reliant on identifying harvested and
non-harvested organisms and their products (Ovenden
et al. 2015). Correct species identification is essential
to define the species composition of a fishery, identify
by-catch (whether retained or discarded), delineate
distribution ranges and to assess fishery stocks. Correct
species identification is challenging for fishers, managers,
compliance officers and researchers alike, particularly
for shark species with little phenotypic variation, such as
carcharhinids (Tillett et al. 2012a). Of particular concern is
that most fisheries do not undertake species identification
in catch statistics and sharks are often grouped into
generic categories (FAO 2011). Furthermore, sharks are
primarily processed at sea where the main morphological
characteristics used to identify sharks to the species level,
such as heads and fins, are removed. Without correct
species identification information, the impact that fisheries
could have on individual species is largely unknown.
Non species-specific reporting of chondrichthyans
Generic reporting for elasmobranch catches in South
African fisheries is a common practice. Dogfish Squalus
spp., skates Raja spp., shysharks Haploblepharus
spp. are all listed in generic groups (Attwood et al.
2011; Best et al. 2013). Processed spotted gully sharks
(Triakis megalopterus Smith, 1839), tope sharks and two
smoothhound species M. mustelus, M. palumbes are all
referred to as gummy or hound sharks. Bronze whaler
(or copper) sharks, dusky sharks and blacktip sharks
(Carcharhinus limbatus Müller and Henle, 1839) are
processed and all sold under the name bronze whalers
(da Silva and Bürgener 2007).
For chondrichthyans that are listed to the species level,
there is also potential for misidentification in fisheries
records. Whitespotted smoothhounds, dusky sharks and,
although in small numbers, sandbar sharks (Carcharhinus
plumbeus Nardo, 1827) have all been documented in
fisheries in False Bay (Lamberth 2006; da Silva and
Bürgener 2007). None of these species, however, were
reported in fisheries survey and catch data, possibly due
to misidentification as other species or generic fisheries
reporting (Best et al. 2013). Furthermore, all Squalus
species occurring along the southern African coast are
lumped into Squalus spp. records including the two
most common species, Squalus acutipinna (formerly S.
megalops Macleay, 1881) and S. cf. mitsukurii, as well
as an offshore species, Squalus acanthias Linnaeus,
1758. Many of the Squalus species have previously been
 African Zoology 2015: 1–13 3

Table 1: Shark species affected by South African fisheries: International Union for the Conservation of Nature (IUCN) Redlist status, where
DD  Data Deficient, NT  Near Threatened, V  Vulnerable, E  Endangered, estimated catch of 2010 in tons and main fishery sectors
impacting on the respective species (DAFF 2013). Species in bold denote sharks endemic to southern Africa. Trawl  inshore, offshore,
midwater and prawn trawl; Linefish  traditional linefishery; Shark longline  demersal and pelagic shark longline; Hake longline  hake
longline fishery; Tuna longline  tuna and swordfish pelagic longline (DAFF 2013)

Estimated catch
Family Species IUCN status Main directed fisheries Main by-catch fisheries
2010 (t)
Hexanchidae Notorynchus cepedianus DD 1–10 Shark longline, Linefish –
Carcharhinidae Carcharhinus brachyurus NT 201–300 Shark longline, Linefish Hake longline, Trawl
Carcharhinus obscurus VU 11–100 Shark longline, Linefish Hake longline, Trawl
Carcharhinus limbatus NT 1–10 Shark longline –
Prionace glauca NT 301–400 Pelagic longline Tuna pole
Triakidae Galeorhinus galeus VU 401–500 Shark longline, Linefish Hake longline, Trawl
Mustelus mustelus VU 300–400 Shark longline, Linefish Hake longline, Trawl
Mustelus palumbes DD 11–100 Shark longline, Linefish Hake longline, Trawl
Mustelus mosis DD 1–10 Shark longline, Linefish Hake longline, Trawl
Triakis megalopterus NT 1–10 Shark longline, Linefish Hake longline, Trawl
Sphyrnidae Sphyrna zygaena VU 1–10 Shark longline Linefish, Tuna longline
Sphyrna lewini EN 1–10 Shark longline Linefish, Tuna longline
Downloaded by [RMIT University] at 07:49 17 August 2015

Sphyrna mokarran EN 1–10 Shark longline Linefish, Tuna longline

Lamnidae Isurus oxyrinchus VU 501–600 Pelagic longline Tuna pole
Squalidae Squalus acutipinna DD 11–100 – Trawl, Hake longline
Scyliorhinidae Halaelurus natalensis DD 1–10 – Trawl, Hake longline
Haploblepharus edwardsii NT 1–10 – Trawl, Shark longline
Haploblepharus fuscus VU 1–10 – Trawl
Haploblepharus pictus LC 1–10 – Trawl
Holohalaelurus regani LC 1–10 – Trawl, Hake longline
Poroderma africanum NT 1–10 – Trawl, Shark longline
Poroderma pantherinum DD 1–10 – Trawl, Shark longline
Scyliorhinus capensis NT 1–10 – Trawl
Callorhinchidae Callorhinchus capensis LC 801–900 St Joseph net Trawl

misidentified (Naylor et al. 2012) and the genus is under
ongoing revision. Without species-specific data, population
trends and accurate fisheries data cannot be assessed.
Due to the difficulty in identifying chondrichthyans to the
species level, particularly postharvest, genetic techniques
can be used to assist in this pursuit.
Seafood fraud and illegal trade
Recently, there has been considerable interest and
concern surrounding the mislabelling of fishery products,
both globally and locally. Helyar et al. (2014), for example,
reported on seafood mislabeling in the UK and highlighted
the importance of genetic testing across the supply chain
with the ultimate goal of achieving sustainability of exploited
marine resources. A high incidence (31%) of mislabelling
of South African commercial fish products and species
substitution and fraud has been found (Cawthorn et al.
2012). Although this study did not detect any substitution
with shark meat per se, according to the Southern Africa
Sustainable Seafood Initiative (SASSI) fish retailers
are increasingly selling unlabelled or mislabelled shark
products due to its unpopularity with local consumers
(Atkins 2010). Shortfin mako sharks, for example, are being
renamed and sold as gummy, lemon fish or ocean fillets
to increase its consumer appeal and to disguise allowable
catch limits (Atkins 2010). DNA barcoding, for example,
revealed a high incidence of seafood fraud in Italian
commercial shark fillets (Barbuto et al. 2010). Lucrative
Mustelus species were substituted with the less valuable
spiny dogfish (Squalus acanthias), shortfin mako (Isurus
oxyrinchus Rafinesque, 1810) and blue shark (Prionace
glauca Linnaeus, 1758) meat in 77% of samples tested.
Similarly, in a small-scale study testing 20 commercial
samples taken from different Spanish supermarkets, only
20% of ray species (Raja spp.) were correctly labelled
(Lago et al. 2012). To date, no studies have been
conducted to assess the accuracy of labelling of shark
products in South Africa. Since most of the aforementioned
species are prevalent and caught by fisheries along the
southern African coast, simple but sensitive molecular tests
will aid in monitoring local shark fisheries and enhance
transparency on the domestic market.
Despite a growing movement of regional, national
and international regulations and management of shark
species, there is evidence of continued trade in protected
species. Approximately 5% of shark fillets sampled at
markets, supermarkets, street vendors and in restaurants in
Taiwan were identified as species listed in the Convention
on International Trade in Endangered Species of Wild
Fauna and Flora (CITES) Appendix II, including two
species of hammerhead Sphyrna spp., oceanic white tip
(Carcharhinus longimanus Poey, 1861) and white shark
(Carcharodon carcharias Linnaeus, 1758) (Liu et al. 2013).
A high incidence (55% of all samples tested) of the critically
endangered largetooth sawfish (Pristis pristis Linnaeus,
1758) were found in Brazilian fish markets (Melo Palmeira
et al. 2013) and almost one-third of fish samples tested for
species substitution in Italian fish markets included white
 4 Bester-van der Merwe and Gledhill
shark (Filonzi et al. 2010). Of similar concern is the growing
demand for the Asian shark fin market that is undoubtedly
a major contributor to the global shark trade (Clarke et
al. 2005, 2006). The number of fins obtained from Illegal,
Unreported and Unregulated (IUU) sources is estimated to
be three to four times the amount of reported catch data
(Clarke et al. 2006). In southern Africa, illegal shark finning
continues to be problematic, despite legislation prohibiting
the activity (da Silva et al. 2015).
Taxonomic identification and confusion
There is confusion around the identification and taxonomy
of some of the smaller, demersal sharks in South African
waters, including Mustelus and Haploblepharus species.
It has been proposed that there is potential for cryptic
species and/or hybrids within these genera (Human 2007).
Off the southern African coast, there are three Mustelus
species found: Mustelus mustelus, M. palumbes and
hardnose smoothhound (Mustelus mosis Hemprich and
Downloaded by [RMIT University] at 07:49 17 August 2015
Ehrenberg, 1899) (Smale and Compagno 1997). Mustelus
mustelus and M. palumbes are overlapping in distribution,
whereas M. mosis rarely occurs on the east coast. Although
M. palumbes is fairly easily distinguishable from M. mustelus,
there is a lack of species-specific data and identification
remains problematic, especially for juveniles. Fisheries,
population and distribution data for these sharks may be
confounded due to misidentification between the species.
The identification and nomenclature of Mustelus species
are also problematic globally (White and Last 2006, 2008;
Farrell et al. 2009; Boomer et al. 2012; Velez-Zuazo et al.
2015). Based on a combination of microsatellites and mtDNA
forensic markers, species misidentification of Mustelus
spp. by a South African commercial fishing company was
recently revealed. Fifty-nine hound shark samples were
morphologically identified as G. galeus or ‘vaalhaai’ (the
local Afrikaans common name for soupfin sharks) (Maduna
2014). Using cytochrome oxidase subunit 1 (CO1) barcoding
analysis, only 25 were confirmed to be G. galeus, whereas
20 were revealed as M. mustelus and a further four as
M. palumbes (Maduna 2014). This highlights the difficulty
in distinguishing between these commercial species and
how species-specific catch data can be subsequently
misrepresented in commercial fisheries records. Further
studies need to be conducted to determine the degree of this
misidentification in all fisheries sectors in South Africa.
Apart from identification issues that relate to known
species, classification of cryptic or newly described
species is complicated. A holistic approach combining
genetic and morphometric data is essential. With such
great elasmobranch diversity in the Southern Hemisphere,
taxonomic problems exist for the smaller demersal and
benthopelagic species with high prevalence of cryptic
species complexes, as well as for many deep-sea species
vulnerable to offshore fishing pressures (Straube et al. 2010;
Dudgeon et al. 2012). Other than the Mustelus species, the
family Scyliorhinidae (catsharks) is also considered as one
of the most systematically troublesome taxonomic groups.
A high degree of morphological conservatism is observed in
the genus Haploblepharus (Human 2003, 2007).
Four Haploblepharus species are found in South Africa.
Three species are endemic to South Africa; puffadder
shysharks (Haploblepharus edwardsii Schinz, 1822), brown
shysharks (H. fuscus Smith, 1950) and Natal shysharks
(H. kistnasamyi Human and Compagno, 2006), whereas
the dark shyshark (H. pictus Müller and Henle, 1838) is also
found in Namibia (Compagno et al. 2005). The poor choice
of morphological characteristics, including colour patterns,
in species identification keys (Human 2007) has potentially
led to the over- and/or under-estimation of the abundance
of these species and confusion over the distribution
ranges. Juvenile specimens are difficult to identify and it
is possible that hybridisation may occur between species
of this genus, further complicating species identification
(Human 2007). Correct identification of Haploblepharus
species is of conservation importance due to differences
in IUCN Redlist classifications of each of the species. All
species are listed on the IUCN Redlist under the following
categories: H. kistnasamyi – Critically Endangered;
H. fuscus – Vulnerable; H. edwardsii – Near Threatened;
and H. pictus – Least Concern (Table 1). There is a need
for phylogenetic analysis and a revision of morphological
characters to clarify the relationships between species of
this group (Human et al. 2006). Molecular markers could be
used to re-evaluate species separation in Haploblepharus
and confirm whether the current morphological characters
used in taxonomic keys should be reassessed. This will
aid in the conservation and management of the southern
African shyshark species.
Molecular tools for species identification
Currently, the most frequently used genetic tool in species
identification is DNA barcoding, in which a standardised
DNA fragment, typically mitochondrial DNA, is sequenced
and compared against a reference database in order to
identify or ‘fingerprint’ a particular species (Hebert et al.
2003). DNA barcoding of elasmobranchs is primarily based
on a single fragment of the CO1 mitochondrial gene with
a length of 648 bp. Results from a variety of animal taxa
show that the CO1 gene has been effective in distinguishing
between 95% of species (Hebert et al. 2003; Ward et al.
2005; Hajibabaei et al. 2006). DNA barcoding using the CO1
gene has been used to successfully identify fish species
(Ward et al. 2005, 2008; Hubert et al. 2008; Steinke et al.
2009), including shark species (Holmes et al. 2009; Wong et
al. 2009; Ward 2009; Moftah et al. 2011; Moura et al. 2015).
The efficiency of the CO1 gene region for identification of
many chondrichthyans at a species-specific level remains
untested and currently there is some uncertainty about the
use of this region as a universal DNA barcoding gene for
chondrichthyans (Daley et al. 2012; Naylor et al. 2012). The
limitation of this region was demonstrated in a recent study
that evaluated the suitability of the CO1 region for species
identification in three co-occurring Haploblepharus species,
H. edwardsii, H. pictus and H. fuscus. The between-
species CO1 nucleotide variation was extremely low and
could, for example, not discriminate the taxonomically
identified H. fuscus specimens from the H. pictus specimens
(Robbertze unpublished data).
There are open-access public reference databases,
such as the Barcode of Life Database (BOLD; http://www.
boldsystems.org), FISH-BOL (http://www.fishbol.org) and
GenBank (http://www.ncbi.nlm.nih.gov/genbank), for storing
 African Zoology 2015: 1–13 5

and matching genetic data. The BOLD and FISH-BOL
databases are part of the International Consortium of the
Barcode of Life initiative (http://www.ibol.org). The BOLD
database consists of several recognised DNA barcoding
genes with high-quality assurance requirements, whereas
GenBank is a repository for all available DNA sequences.
While using barcoding as a tool for identifying verified
species is well accepted, it’s use in ‘discovering’ new
species and assigning taxonomic placements based solely
on genetic data remains controversial (DeSalle et al.
2005; DeSalle 2006). DNA barcoding should be a tool to
accompany and complement taxonomy.
Classical taxonomy screens numerous individuals
from multiple localities across the range of a species
to distinguish variation within a species from variation
between species (DeSalle et al. 2005). This same
approach needs to be applied for barcoding data. At
present, global reference databases, such as BOLD or
FISH-BOL, are incomplete and multiple entries exist
Downloaded by [RMIT University] at 07:49 17 August 2015
et al. 2015). Barcoding data are available for almost 70%
of the 66 extant shark species found in southern African
waters, with multiple entries in BOLD for the majority of the
cosmopolitan species (Figure 1). However, less than 50%
of southern African endemic species have been barcoded.
The integrity of the barcode data available through
online databases is dependent on the correct identification
of the specimen that was sampled. Since 35% of the
southern African species are considered rare (i.e. less
than 10 records), taxonomic clarity through morphometric
identification, photographic identification, detailed specimen
and collection data to accompany the genetic data is
essential to ensure the accuracy of reference barcode
data. Barcode sequences should be accompanied by
voucher specimens deposited in museums or, at the very
least, voucher photographs considering the logistical
challenges associated with the preservation and archival
of large-bodied animals such as sharks (Doukakis et
al. 2011). It is recommended that nucleotide sequence

primarily for cosmopolitan species. Multiple entries from similarity searches against reference databases should
different regions for each species will improve the accuracy be performed using the BOLD database (restricted to
of these databases (Dudgeon et al. 2012; Velez-Zuazo taxonomically validated specimens) in preference to

Endemics regional 49%

Species barcoded

66% Taxonomic records

Chondrichthyans regional

Carcharhiniformes global 78%

Orectolobiformes global 91%

Heterodontiformes global 75%

Lamniformes global 88%

Hexanchiformes global 100%

Squaliformes global 82%

Squatiniformes global 90%

Pristiformes global 55%

Pristiophoriformes global 60%

77%
Rajiformes global

Torpediniformes global 85%

Chimaeriformes global 94%

0 100 200 300 400 500

NUMBER OF SPECIES

Figure 1: Percentage of recorded chondrichthyan species with DNA barcodes available in the Barcode of Life Database (BOLD).
Southern African fauna and endemics (depicted as ‘regional’) are compared with the total number of DNA barcodes (‘global’) available for
12 of the 13 orders
 6 Bester-van der Merwe and Gledhill
GenBank, in order to ensure success and accuracy of
species identification (Helyar et al. 2014).
Molecular species identification is not restricted to
barcoding and several other markers and approaches have
sufficient discriminatory power in chondrichthyans. Using
a 1 044 bp fragment of the mitochondrial NADH2 gene,
Naylor et al. (2012) identified 574 species of elasmobranchs
(305 sharks and 269 batoids), representing 56 of the 57
described families. Similarly, multiplex-PCR (Farrell et al.
2009), restriction fragment length polymorphism (RFLPs),
PCR-RFLPs (Mendonça et al. 2009) and amplified fragment
length polymorphisms (AFLPs) (Zenger et al. 2006) have
also been used in shark species identification.
The South African National Plan of Action for the
Conservation and Management of Sharks (hereafter
referred to as SA NPOA-Sharks) has identified that there
are gaps in the knowledge of the taxonomy and classifi-
cation of South Africa’s shark species (DAFF 2013). The
SA NPOA-Sharks has listed the reclassification of all
Downloaded by [RMIT University] at 07:49 17 August 2015
rays, skates and deepwater shark species using morpho-
metrics and genetics as an immediate priority (DAFF
2013). Acquiring baseline barcode data of all South
African chondrichthyans should be a research and funding
priority. Reference barcode data for all described South
African species are urgently needed so that samples from
an undetermined species can be compared to reference
barcode databases. Barcoding the South African endemic
species needs to be a priority, as less than half of the
species have been barcoded.
Similarly, molecular genetic tools can be used to identify
species of conservation concern postharvest and in
processed products available in the commercial market,
including meat, fins and even in processed, multi-species
products, such as shark cartilage pills (Chapman et al.
2003). Species-specific assays using multiplex PCR
reactions incorporating species-specific primers targeting
the nuclear ribosomal RNA internal transcribed spacer 2
(rRNA ITS2) and mitochondrial cytochrome b (cytb) have
been developed to identify sharks of conservation concern
in the shark fin market, such as white sharks (Chapman
et al. 2003), three hammerhead species listed in CITES
Appendix II (Abercrombie et al. 2005), and basking sharks
(Cetorhinus maximus Gunnerus, 1765) (Magnussen et
al. 2007). This is a rapid, low-cost technique that requires
only PCR and distinguishes between multiple species
simultaneously (Abercrombie et al. 2005). As such, this
technique is suitable for use in developing countries, such
as southern African nations, where financial restraints may
limit large-volume sequencing.
Evidence of cryptic speciation and hybridisation of
elasmobranchs is emerging, further complicating taxonomic
assessment and species identification. The first documented
naturally occurring shark hybrids between two sympatric
blacktip shark species of the genus Carcharhinus were
recently confirmed, using a combination of morpho-
logical characteristics and DNA-based diagnostic markers
(Morgan et al. 2012). Subsequently, the first wild hybrid
individual of two Manta species (Walter et al. 2013) and
hybridisation between two freshwater stingrays has been
identified (Cruz et al. 2015). Two co-occurring Mustelus
species, M. mustelus and M. punctulatus, in the Adriatic Sea
also showed signs of hybridisation and/or gene introgression
when tested for the nuclear codominant marker ITS2 to
evaluate reproductive interactions (Di Francesco 2011).
Taking into account the similar reproductive modes for at
least two of the Mustelus species present in southern
Africa (Boomer et al. 2012), hybridisation is a possibility.
DNA-based identification together with morphological data,
such as stretched total length (STL), pre-caudal length
(PCL) and vertebral counts (Morgan et al. 2012), could
verify the occurrence of hybrids or potential hybrid zones
that need to be maintained and ideally managed separately
from the parental species. Clarification of the taxonomy and
identification of the Mustelus spp. and Haploblepharus spp.
is imperative due to the commercial importance of Mustelus
spp. in South Africa and the varying threatened statuses of
these species. Identifying the presence of cryptic species or
hybrids using a combination of morphological and genetic
techniques will determine whether this is contributing to
taxonomic confusion in these species (Dudgeon et al. 2012;
Morgan et al. 2012).
Population structure assessment for shark fisheries
management
Population genetic analysis at and below the species
level forms an important basis for species conservation
and sustainable exploitation through the identification of
the number of stocks and management units within the
geographical distribution of a target species (Ovenden
et al. 2009). In fisheries, the stock concept is directly
linked to the management of populations or units that are
ecologically separated through space and time (Waples
1998). Correct identification of genetically differentiated
stocks is vital for the proper management of exploited
species and the preservation of their genetic diversity,
and the genetic integrity of individual species. Despite the
absence of obvious barriers to gene flow, most fish species
do not comprise a single-continuously distributed, panmictic
population of individuals (Hemmer-Hansen et al. 2007). In
the past, the extent of genetic differentiation between shark
populations was expected to be low due to their capacity
to move extensively, however, several studies have
shown different levels of population genetic subdivision
over large and smaller spatial scales (e.g. Dudgeon et al.
2009; Ovenden et al. 2009; Feldheim et al. 2010; Geraghty
et al. 2013). Population genetic structure can range from,
for example, basking sharks that display little genetic
differentiation over ocean basins globally (Hoelzel et al.
2006) to blacktip sharks that show significant structure
over small, regional scales (Keeney et al. 2005; Sodré
et al. 2012). At present, carcharhinids have the greatest
representation in the phylogeographic literature, as many of
these species are of economic importance in commercial,
recreational and artisanal fisheries (Dudgeon et al. 2012).
These species, however, may have been studied in greater
detail due to the fact that it is easier to obtain access to
a sufficient number of samples of the species that are
encountered through fisheries.
Along the southern African coast, the warm Agulhas
Current and the cold Benguela Current have a strong
influence on marine populations of the east and west
 African Zoology 2015: 1–13
coast of southern Africa, respectively (Hutchings et al.
2009). It has recently been proposed that the physiological
features and dynamics between these two ocean currents,
together with climate oscillation, are the major driving
forces behind the historical and contemporary restriction
of gene flow across the Indian/Atlantic boundary (Teske et
al. 2013). Despite the uncertainty of the exact mechanism,
this Indian/Atlantic boundary is evident in many globally
distributed species as well as in a number of coastal fishes
around southern Africa (Henriques et al. 2012, 2014),
where the Benguela Current has shown to have a strong
influence on the magnitude and directionality of gene flow.
Signatures of historical gene flow across the boundary
during warm interglacial periods (Peeters et al. 2004) and
evidence for intensification of the Agulhas leakage due to
climate change and a weaker Agulhas Current (Biastoch
et al. 2008; van Sebille et al. 2009) could explain the
lesser degree of genetic distinctness between the west
and east coast populations for some species, as well as
Downloaded by [RMIT University] at 07:49 17 August 2015
the presence of a transition/admixture zone for some.
For example, the Benguela barrier does not appear to
be a genetic barrier to temperate shark species, such as
Carcharhinus brachyurus (Benavides et al. 2011) and
Galeorhinus galeus (Chabot and Allen 2009). In a recent
study, microsatellites revealed strong genetic differentiation
between South-east Atlantic and South-west Indian Ocean
Mustelus mustelus, indicating that for this smaller coastal
shark, the Indian/Atlantic boundary (Teske et al. 2013)
most likely restricts contemporary gene flow (Maduna
2014). Interestingly, mtDNA sequence data for the same
species found relatively high levels of interoceanic gene
flow and these differential genetic signals reflected by the
two molecular marker types was attributed to either gender-
biased dispersal or the more conservative evolutionary
properties inherent to mitochondrial DNA markers as
apposed to microsatellites (Maduna 2014).
Reproductive philopatry and resultant gender-biased
dispersal is another mechanism that can account for
population structure, despite the absence of barriers to
movement (Dudgeon et al. 2012; Chapman et al. 2015).
Reproductive philopatry, where females show site-fidelity
to nursery grounds, has been identified in numerous
coastal, viviparous shark species using a combination
of microsatellites and mtDNA sequence data (Feldheim
et al. 2002; Keeney et al. 2005; Karl et al. 2011; Tillett
et al. 2012b). Importantly, the spatial scale at which
philopatry occurs varies between species, thereby further
contributing to differential genetic structuring patterns
observed amongst species. Identifying critical areas within
a species’ distribution range, such as nursery sites, could
make a strong case for giving these areas special attention
(Mourier and Planes 2013; Feldheim et al. 2014). In South
Africa, many coastal embayment or river mouth areas such
as Storms River, Algoa Bay and Thukela River have been
identified as nursery grounds for shark species (Smale
2002; Dicken 2008; Hussey et al. 2009). We need to gain
a greater understanding of the behavioural dynamics of
shark populations in these areas and how these processes
may affect the genetic structure of a species, particularly
for commercially important species, in order to identify
areas of critical protection.
7
Molecular tools for population structure and
demographic assessment
Several molecular marker types are available for assessing
gene flow patterns of organisms with different life-history
traits and dispersal capabilities. In sharks, genetic
variation is known to be low, with mitochondrial sequence
evolution estimated to be six to eight times slower than
that of mammals (Martin et al. 1992). Despite this, a
number of studies have been successful in assessing
population differentiation in sharks using a portion of the
mitochondrial control region (mtCR) (Keeney et al. 2005;
Keeney and Heist 2006; Duncan et al. 2006; Chabot
and Allen 2009; Sodré et al. 2012). Microsatellites, or
simple sequence repeats (SSRs), have also been used
and these highly variable short, tandem repeat DNA
sequences have proven to be ideal for fine-scale stock
structure investigations relevant to short-term fisheries
management in sharks (Dudgeon et al. 2012). Although
several species-specific microsatellite markers have been
isolated and characterised for elasmobranch species (see
Portnoy and Heist 2012) and cross-species transferability
of microsatellites has been successful (Boomer and
Stow 2010; Chabot and Nigenda 2011; Maduna et al.
2014), very few studies have assessed genetic structure
of sharks and other elasmobranchs along the South
African shoreline (Table 2). While a number of global or
cross-oceanic studies of cosmopolitan species included
samples from southern Africa, only a few studies sampled
both the Atlantic and Indian coastlines of the region and
could test, for example, the validity of the Benguela barrier
as a barrier to dispersal. The effect of biogeographic
barriers on the genetic structure of smaller, demersal and
inshore-dwelling shark species is still largely unknown
and warrants further investigation. Oceanographic
features, such as ocean currents and thermal fronts, may
have varying degrees of impact on species with different
ecology and life-history traits. Preliminary investigation
into the genetic structure of two demersal shark species
targeted in regional fisheries, tope sharks and common
smoothhounds, has revealed substantial differences in the
degree of population differentiation (Bitalo et al. 2015). This
highlights the importance of considering species-specific
gene flow patterns in fisheries management practices
and stock assessments. The Draft South African Shark
Biodiversity Management Plan has identified the need for
population genetic studies on sharks and has stated one
of its objectives is ‘to improve knowledge of population
delineation and genetic diversity of identified shark species’
(RSA 2014: 27).
The South African coastline has recently been
redefined as holding as many as nine marine bioregions,
that incorporate both previously recognised coastal
biogeographic regions, as well as newly demarcated
offshore regions (Griffiths et al. 2010). Given the diversity
of biogeographic regions and the many unique habitats
that sharks inhabit along the South African coastline,
such as the Langebaan Lagoon on the West Coast and
the Breede and Umfolozi Rivers, it is imperative for
the management and conservation of these species to
understand whether these areas hold unique breeding and
reproductive stocks (da Silva et al. 2013). Investigation
 8 Bester-van der Merwe and Gledhill

Table 2: Studies involving population structure analysis of shark species targeted in South African fisheries. Information given includes
the study area investigated, whether samples from southern Africa were included (SA samples), type and number of molecular
markers used (mtDNA and nuclear), the population genetic structure found and references. mtCR  mitochondrial control region,
ND2  nicotinamide adenine dehydrogenase subunit 2, ND4  nicotinamide adenine dehydrogenase subunit 4, SSRs  short sequence
repeats or microsatellites

SA samples Markers used

Species Study area Genetic structure Reference
included mtDNA Nuclear
Carcharhinus brachyurus Global Yes mtCR – Inter-oceanic Benavides et al. (2011)
Carcharhinus obscurus Australia No mtCR 4 SSRs Regional, only mtCR Ovenden et al. (2009)
Carcharhinus limbatus North-western Atlantic No mtCR 8 SSRs Regional, both markers Keeney et al. (2005)
Global Yes mtCR – Across Atlantic Keeney and Heist (2006)
Western Atlantic No mtCR – Regional, western Atlantic Sodré et al. (2012)
Prionace glauca Global – mtCR 16 SSRs Across equator Fitzpatrick (2012)
Galeorhinus galeus Global Yes mtCR – Inter-oceanic Chabot and Allen (2009)
South Africa Yes ND2 22 SSRs Low to absent Bitalo (unpublished data)
Global Yes ND2 22 SSRs Inter-oceanic Bitalo (unpublished data)
Mustelus mustelus Southern Africa Yes ND4 12 SSRs Atlantic-Indian Maduna (2014)
Triakis megalopterus Southern Africa Yes mtCR 6 SSRs Atlantic-Indian Soekoe (unpublished data)
Sphyrna lewini Global Yes – 13 SSRs Low to absent Daly-Engel et al. (2012)
Downloaded by [RMIT University] at 07:49 17 August 2015

Australia No ND4 8 SSRs Absent Ovenden et al. (2011)

Mexico No mtCR 15 SSRs Regional, both markers Nance et al. (2011)
Isurus oxyrinchus Global No – RFLPs Absent Heist et al. (1996)
Global Yes – 4 SSRs Absent Schrey and Heist (2003)

into the genetic stock structure of shark species,
particularly species that are affected by fisheries, should
form an integral part of the multidisciplinary approach to
fisheries management. Table 2 shows a summary for the
species for which this has been addressed on a regional
scale and highlights the substantial gaps in the basic
population genetic information for southern African sharks
affected by fisheries.
Similar to population structure inference, molecular
markers and genetics have increasingly been used to
assess reproductive biology and mating behaviour in
sharks. Most notably is the investigation of polyandry
and multiple paternity, using as few as four microsatellite
markers. Multiple paternity has been identified in
numerous shark species (reviewed in Byrne and Avise
2012); however, the benefits of multiple paternity in
sharks is to a large extent still unclear (Daly-Engel et al.
2010; Portnoy and Heist 2012). No evidence of increased
genetic diversity and fitness in multiple-sired litters of
lemon sharks (Negaprion brevirostris Poey, 1868) were
found when compared to singly sired litters (DiBattista et
al. 2008). Karl (2008) demonstrated that multiple paternity
might even lead to a reduction in effective population
size (Ne) by increasing the variance in male reproductive
success. Nonetheless, it is important to know whether
reproductive behaviour is affected in commercially fished
areas and how this behaviour varies across species and
populations. Three species of commercial importance in
South Africa, M. mustelus, S. lewini and C. obscurus, have
been examined for the presence of multiple paternity (MP)
using microsatellite panels optimised for each species
(Rossouw unpublished data). Differences in frequencies
of multiple paternity were observed between species
and coincides with the variation in MP rates previously
observed across species (Boomer et al. 2013). The
differences in MP rates between populations of the same
species should ideally also be assessed to elucidate the
possible effect of fishing on mating behaviour in heavily
fished versus non-fished areas.
Furthermore, the identification of genetic bottlenecks and
any other population size fluctuations due to anthropogenic
pressures, such as overfishing, are of great importance
to management and conservation of marine species.
Populations that are currently large may have had small
long-term Ne due to a genetic bottleneck or population size
decline in the past (Turner et al. 2002). The identification of
present populations with a reduced Ne is therefore essential
for conserving a species’ genetic diversity. Estimating
contemporary Ne for chondrichthyans is important, since
many species are overexploited in fisheries globally
(Musick et al. 2000). The effective population size could
give an indication of both the breeding population size and
the general health of a population (Portnoy et al. 2009). In
particular, understanding the relationship or ratio between
Ne and demographic census sizes can be informative for
management decisions (Dudgeon et al. 2012). Estimates
of Ne can be based on genetic or demographic data, but
since demographic information (e.g. sex ratio, fluctuation
in population size and pedigree data) is often unavailable
for wild populations, current approaches to estimating
effective population sizes are based on indirect methods
using genetic information (Dudgeon et al. 2012). Most
valuable to fisheries management is the development and
utility of single time-point estimations of Ne, in which only a
single sampling of a population is needed. Using molecular
markers, the single time-point method has recently
successfully been applied to estimate Ne in a number of
elasmobranch species (Ahonen et al. 2009; Chapman et al.
2011; Blower et al. 2012). An emphasis should be placed
on effective population size estimates of species that are
particularly vulnerable to exploitation. This could enable the
identification of species or populations that show critically
 African Zoology 2015: 1–13
lower population estimates compared with unexploited
species or populations in protected areas.
Next generation technologies and future investigations
In the last decade, advances in molecular technologies,
such as next generation sequencing (NGS) and
high-throughput genotyping methods, have greatly
facilitated the genetic characterisation in many non-model
organisms (Ekblom and Galindo 2011). With such a diverse
shark biodiversity in southern Africa, these technologies
now also allow for individual species to be characterised on
a genome-wide level at a lower cost. With the many NGS
and high-throughput genotyping platforms now available,
a larger number of molecular markers with a higher
genome representation can be developed and genotyped
in sharks. Single nucleotide polymorphisms (SNPs) are
becoming increasingly popular for genetic applications
due to their abundance in genomes and suitability for
automation (Morin et al. 2009). Novel approaches towards
Downloaded by [RMIT University] at 07:49 17 August 2015
identifying SNPs include the utilisation of these NGS data
sets, followed by various SNP discovery bioinformatics
pipelines, allowing increased throughput while reducing the
cost (Etter et al. 2011). When studying organisms lacking a
reference genome, genome subsampling can be attained
using restriction-site associated DNA (RAD) sequencing,
which creates short DNA fragments that are adjacent to
recognition sites of specific restriction enzymes, resulting
in RAD tag libraries (Etter et al. 2011). The SNPs are
then detected by sequencing the nucleotides next to the
restriction enzyme sites. The RAD sequencing approach
accelerates SNP discovery and, in turn, can be used
to genotype hundreds or thousands of SNP markers in
several individuals across different populations (Etter et al.
2011; Davey et al. 2013). Similarly, larger numbers of SNPs
can also be identified alongside microsatellites through next
generation transcriptome sequencing (Helyar et al. 2012;
Krück et al. 2013).
Transcriptome sequencing enables characterisation
of all transcriptional activity, coding and non-coding, and
can therefore also be applied to study gene expression
and functional variation (Marguerat and Bähler 2010).
In sharks, this can be a powerful tool to investigate, for
example, ecological adaptation of species to certain areas,
such as freshwater or river areas. In addition, comparative
transcriptomics can be useful in assessing important
molecular features associated with physiological and
behavioural differences within species, thereby examining
various hydrological and temperature regimes as well as
biogeographic zones across the southern Africa coastline.
Conclusion
A growing concern for declining shark populations, coupled
with an increase in South Africa’s shark fisheries, means
that shark populations and stocks need careful monitoring
in order to achieve sustainable utilisation of this fisheries
resource. Species- and population-specific information
is imperative to reach this goal. Together with traditional
fisheries management measures, genetic techniques can
be used for a wide range of chondrichthyan conservation
and management applications. Molecular tools can assist
9
in species identification by elucidating species composition
of fisheries, identifying by-catch, and identifying fisheries
products postharvest. Genetic data can be used for
compliance and enforcement purposes, and to identify
species of conservation concern, such as those protected
by national legislation (e.g. the South African Marine
Living Resources Act; RSA 1998) or international trade
conventions (e.g. CITES). Evidence of mislabelling
or seafood fraud, and fishing and trade in protected
species, can be gathered and used in prosecution cases.
In addition, variation in patterns of genetic structuring
among different shark species has been demonstrated
and genetics is increasingly being incorporated into stock
structure assessment in fisheries. Our present knowledge
of the genetic structure and connectivity of southern
Africa’s shark populations on a national and regional scale
is scarce, and only a few studies have evaluated population
differentiation across known biogeographical barriers.
More information is urgently needed, and both the South
African NPOA-Sharks (DAFF 2013) and the South African
Draft Shark Biodiversity Management Plan (RSA 2014)
identify the need to employ genetics to assist with stock
structure analysis. Historically, the great expense of genetic
technologies has limited research in developing nations
and the exciting transition towards NGS and genome-wide
research will see greater development and application of
genetic research on a regional scale. The declining costs
in equipment and reagents, coupled with advances in
knowledge, techniques and high-throughput technologies,
is making the field more affordable and more tangible
for scientists and managers from developing nations.
The integration of genetic research, development and
application will assist scientists, managers, government
and compliance agencies in closing these gaps in current
knowledge. This will contribute to an integrated approach
to conservation and management of chondrichthyan
populations in southern Africa and aid in the future
sustainability of this fishery resource.
Acknowledgements — We would like to acknowledge Simo
Maduna, Daphne Bitalo and Charné Rossouw for laboratory work
and for generating the genetic data that was used for the prelimi-
nary results and unpublished data mentioned in this study. We
thank the Department of Agriculture Forestry and Fisheries, South
African Shark Conservancy, the KwaZulu-Natal Sharks Board
and the Port Elizabeth Museum, especially Charlene da Silva,
Meaghen McCord, Malcolm Smale, Sabine Wintner and Tamzyn
Zweig for collaboration and for providing valuable information and
samples that made the theme of this manuscript possible. We
thank the anonymous reviewers, whose constructive comments
improved the final version of this manuscript. Financial support was
provided by the the National Research Foundation, South Africa.
References
Abercrombie DL, Clarke SC, Shivji MS. 2005. Global-scale genetic
identification of hammerhead sharks: application to assessment
of the international fin trade and law enforcement. Conservation
Genetics 6: 775–788.
Ahonen H, Harcourt RG, Stow AJ. 2009. Nuclear and mitochondrial
DNA reveals isolation of imperilled grey nurse shark populations
(Carcharias taurus). Molecular Ecology 18: 4409–4421.
Aschliman NC, Ebert DA, Compagno LJ. 2010. A new legskate
 10
(Rajoidei: genus Cruriraja) from southern Africa. Copeia 3:
364–372.
Atkins H. 2010. You could be eating shark meat and not even
know it. Cape Times, 14 May.
Attwood CG, Petersen SL, Kerwath SE. 2011. Bycatch in South
Africa’s inshore trawl fishery as determined from observer
records. ICES Journal of Marine Science 68: 2163–2174.
Barbuto M, Galimberti A, Ferri E, Labra M, Malandra R, Galli P,
Casiraghi M. 2010. DNA barcoding reveals fraudulent substitu-
tions in shark seafood products: the Italian case of “palombo”
(Mustelus spp.). Food Research International 43: 376–381.
Benavides MT, Feldheim KA, Duffy CA, Wintner S, Braccini
JM, Boomer J, Huveneers C, Rogers P, Mangel JC, Alfaro-
Shigueto J, Cartamil DP, Chapman DD. 2011. Phylogeography
of the copper shark Carcharhinus brachyurus in the southern
hemisphere: implications for the conservation of a coastal apex
predator. Marine and Freshwater Research 62: 861–869.
Best LN, Attwood CG, da Silva CD, Lamberth SJ. 2013.
Chondrichthyan occurrence and abundance trends in False Bay,
South Africa, spanning a century of catch and survey records.
African Zoology 48: 201–227.
Downloaded by [RMIT University] at 07:49 17 August 2015
Biastoch A, Böning CW, Lutjeharms JRE. 2008. Agulhas leakage
dynamics affects decadal variability in Atlantic overturning
circulation. Nature 456: 489–492.
Bitalo DN, Maduna SN, da Silva C, Roodt-Wilding R, Bester-van
der Merwe AE. In press. Differential gene flow patterns for
two commercially exploited shark species, tope (Galeorhinus
galeus) and common smoothhound (Mustelus mustelus) along
the south-west coast of South Africa. Fisheries Research.
DOI: 10.1016/j.fishres.2015.07.003.
Blower DC, Pandolfi JM, Bruce BD, Gomez-Cabrera MDC, Ovenden
JR. 2012. Population genetics of Australian white sharks reveals
fine-scale spatial structure, transoceanic dispersal events and low
effective population sizes. Marine Ecology Progress Series 455:
229–244.
Boomer JJ, Harcourt RG, Francis MP, Stow AJ. 2012. Genetic
divergence, speciation and biogeography of Mustelus (sharks) in
the central Indo-Pacific and Australasia. Molecular Phylogenetics
and Evolution 64: 697–703.
Boomer JJ, Harcourt RG, Francis MP, Walker TI, Braccini JM,
Stow AJ. 2013. Frequency of multiple paternity in gummy shark,
Mustelus antarcticus, and rig, Mustelus lenticulatus, and the
implications of mate encounter rate, post-copulatory influences,
and reproductive mode. Journal of Heredity 104: 371–379.
Boomer JJ, Stow AJ. 2010. Rapid isolation of the first set of
polymorphic microsatellite loci from the Australian gummy shark,
Mustelus antarcticus and their utility across divergent shark taxa.
Conservation Genetic Resources 3: 393–395.
Byrne RJ, Avise JC. 2012. Genetic mating system of the brown
smoothhound shark Mustelus henlei, including a literature review
of multiple paternity in other elasmobranch species. Marine
Biology 159: 749–756.
Cawthorn DM, Steinman HA, Witthuhn RC. 2012. DNA barcoding
reveals a high incidence of fish species misrepresentation
and substitution on the South African market. Food Research
International 46: 30–40.
Chabot CL, Allen LG. 2009. Global population structure of the tope
Galeorhinus galeus inferred by mitochondrial control region
sequence data. Molecular Ecology 18: 545–552.
Chabot CL, Nigenda S. 2011. Characterization of 13 microsatellite
loci for the tope shark, Galeorhinus galeus, discovered with
next-generation sequencing and their utility for eastern Pacific
smooth-hound sharks (Mustelus). Conservation Genetic
Resources 3: 553–555.
Chapman DD, Abercrombie DL, Douady CJ, Pikitch EK, Stanhopen
MJ, Shivji MS. 2003. A streamlined, bi-organelle, multiplex PCR
approach to species identification: application to global conserva-
tion and trade monitoring of the great white shark, Carcharodon
Bester-van der Merwe and Gledhill
carcharias. Conservation Genetics 4: 415–425.
Chapman DD, Feldheim KA, Papastamatiou YP, Hueter RE.
2015. There and back again: a review of residency and return
migrations in sharks, with implications for population structure
and management. Annual Review of Marine Science 7: 547–570.
Chapman DD, Simpfendorfer CA, Wiley TR, Poulakis GR, Curtis
C, Tringali M, Carlson JK, Feldheim KA. 2011. Genetic diversity
despite population collapsein a critically endangered marine fish:
the smalltooth sawfish (Pristis pectinata). Journal of Heredity
102: 643–652.
Clarke SC, McAllister MK, Michielsens CGJ. 2005. Estimates of
shark species composition and numbers associated with the
shark fin trade based on Hong Kong auction data. Journal of
Northwest Atlantic Fishery Science 35: 453–465.
Clarke SC, McAllister MK, Milner-Gulland EJ, Kirkwood GP,
Michielsens CGJ, Agnew DJ, Pikitch EK, Nakano H, Shivji MS.
2006. Global estimates of shark catches using trade records
from commercial markets. Ecology Letters 9: 1115–1126.
Clarke SC, Milner-Gulland EJ, Bjørndal T. 2007. Social, economic
and regulatory drivers of the shark fin trade. Marine Resource
Economics 22: 305–327.
Compagno LJV. 1999. An overview of chondrichthyan systematics
and biodiversity in southern Africa. Transactions of the Royal
Society of South Africa 54: 75–120.
Compagno LJV, Dando M, Fowler S. 2005. Sharks of the world.
Princeton: Princeton University Press.
Cruz VP, Vera M, Mendonça FF, Pardo BG, Martinez P, Oliveira C,
Foresti F. 2015. First identification of interspecies hybridization
in the freshwater stingrays Potamotrygon motoro and P. falkneri
(Myliobatiformes, Potamotrygonidae). Conservation Genetics 16:
241–245.
DAFF (Department of Agriculture, Forestry and Fisheries). 2013.
National Plan of Action for the conservation and management of
sharks (NPOA-Sharks). Pretoria: DAFF.
Daley RK, Appleyard, SA, Koopman, M. 2012. Genetic catch verifi-
cation to support recovery plans for deepsea gulper sharks
(genus Centrophorus, family Centrophoridae) – an Australian
example using the 16S gene. Marine and Freshwater Research
63: 708–714.
Daly-Engel TS, Grubbs RD, Feldheim KA, Bowen BW, Toonen RJ.
2010. Is multiple mating beneficial or unavoidable? Low multiple
paternity and genetic diversity in the shortspine spurdog Squalus
mitsukurii. Marine Ecology Progress Series 403: 255–267.
Daly-Engel TS, Seraphin KD, Holland KN, Coffey JP, Nance HA,
Toonen RT, Bowen BW. 2012. Global phylogeography with
mixed marker analysis reveals male-mediated dispersal in the
endangered scalloped hammerhead shark (Sphyrna lewini).
PLoS ONE 7: e29986.
da Silva C, Booth AJ, Dudley SFJ, Kerwath SE, Lamberth SJ, Leslie
RW, McCord ME, Sauer WHH, Zweig T. 2015. A description and
updated overview of the status and management of South Africa’s
chondrichthyan fisheries In: Ebert DA, Huveneers C, Dudley SFJ
(eds), Advances in shark research. African Journal of Marine
Science 37. DOI: 10.2989/1814232X.2015.1044471.
da Silva C, Bürgener M. 2007. South Africa’s demersal shark meat
harvest. TRAFFIC Bulletin 21: 55–56.
da Silva C, Kerwath SE, Attwood CG, Thorstad EB, Cowley PD,
Økland F, Wilke CG, Næsje TF. 2013. Quantifying the degree of
protection afforded by a no-take marine reserve on an exploited
shark. African Journal of Marine Science 35: 57–66.
Davey JW, Cezard T, Fuentes-Utrilla P, Eland C, Gharbi K,
Blaxter ML. 2013. Special features of RAD sequencing data:
implications for genotyping. Molecular Ecology 22: 3151–3164.
DeSalle R. 2006. Species discovery versus species identification
in DNA barcoding efforts: response to Rubinoff. Conservation
Biology 20: 1545–1547.
DeSalle R, Egan MG, Siddall M. 2005. The unholy trinity: taxonomy,
species delimitation and DNA barcoding. Philosophical
 African Zoology 2015: 1–13
Transactions of the Royal Society B: Biological Sciences 360:
1905–1916.
DiBattista JD, Feldheim KA, Gruber SH, Hendry AP. 2008. Are
indirect genetic benefits associated with polyandry? Testing
predictions in a natural population of lemon sharks. Molecular
Ecology 17: 783–795.
Dicken ML. 2008. First observations of young of the year and
juvenile great white sharks (Carcharodon carcharias) scaveng-
ing from a whale carcass. Marine and Freshwater Research 59:
596–602.
Di Francesco N. 2011. Species identification, distribution and
reproductive interactions of common smooth-hound and
blackspotted smooth-hound shark (genus Mustelus) in the
Adriatic Sea. MSc thesis, University of Bologna, Italy.
Doukakis P, Hanner R, Shivji M, Bartholomew C, Chapman
D, Wong E, Amato G. 2011. Applying genetic techniques to
study remote shark fisheries in northeastern Madagascar.
Mitochondrial DNA 22: 15–20.
Dudgeon CL, Blower DC, Broderick D, Giles JL, Holmes BJ,
Kashiwagi T, Krück NC, Morgan JAT, Tillett BJ, Ovenden JR.
2012. A review of the application of molecular genetics for
Downloaded by [RMIT University] at 07:49 17 August 2015
fisheries management and conservation of sharks and rays.
Journal of Fish Biology 80: 1789–1843.
Dudgeon CL, Broderick D, Ovenden JR. 2009. IUCN classification
zones concord with, but underestimate, the population genetic
structure of the zebra shark Stegostoma fasciatum in the
Indo-West Pacific. Molecular Ecology 18: 248–261.
Dudley SF, Simpfendorfer CA. 2006. Population status of 14 shark
species caught in the protective gillnets off KwaZulu–Natal
beaches, South Africa, 1978–2003. Marine and Freshwater
Research 57: 225–240.
Dulvy NK, Baum JK, Clarke S, Compagno LJV, Cortés E, Domingo
A, Fordham S, Fowler S, Francis MP, Gibson C, Martínez J,
Musick JA, Soldo A, Stevens JD, Valenti S. 2008. You can swim
but you can’t hide: the global status and conservation of oceanic
pelagic sharks. Aquatic Conservation: Marine and Freshwater
Ecosystems 18: 459–482.
Dulvy NK, Fowler SL, Musick JA, Cavanagh RD, Kyne PM,
Harrison LR, Carlson JK, Davidson LNK, Fordham SV, Francis
MP, Pollock CM, Simpfendorfer CA, Burgess GH, Carpenter KE,
Compagno LJV, Ebert DA, Gibson C, Heupel MR, Livingstone
SR, Sanciangco JC, Stevens JD, Valenti S, White W. 2014.
Extinction risk and conservation of the world’s sharks and rays.
eLife 3: e00590.
Duncan KM, Martin AP, Bowen BW, De Couet HG. 2006. Global
phylogeography of the scalloped hammerhead shark Sphyrna
lewini. Molecular Ecology 15: 2239–2251.
Ebert DA, Cailliet GM. 2011. Pristiophorus nancyae, a new species
of sawshark (Chondrichthyes: Pristiophoridae) from southern
Africa. Bulletin of Marine Science 87: 501–512.
Ebert DA, Compagno LJ. 2007. Biodiversity and systematics of
skates (Chondrichthyes: Rajiformes: Rajoidei). Environmental
Biology of Fishes 80: 111–124.
Ebert DA, Compagno LJ. 2009. Chlamydoselachus africana, a new
species of frilled shark from southern Africa (Chondrichthyes,
Hexanchiformes, Chlamydoselachidae). Zootaxa 2173: 1–18.
Ebert DA, Compagno LJ, De Vries MJ. 2011. A new lanternshark
(Squaliformes: Etmopteridae: Etmopterus) from southern Africa.
Copeia 3: 379–384.
Ebert DA, Haas DL, de Carvalho MR. 2015. Tetronarce cowleyi,
sp. nov., a new species of electric ray from southern Africa
(Chondrichthyes: Torpediniformes: Torpedinidae). Zootaxa 3936:
237–250.
Ebert DA, van Hees KE. 2015. Beyond Jaws: rediscovering the
‘lost sharks’ of southern Africa. In: Ebert DA, Huveneers C,
Dudley SFJ (eds), Advances in shark research. African Journal
of Marine Science 37. DOI: 10.2989/1814232X.2015.1048730.
Ekblom R, Galindo J. 2011. Applications of next generation
11
sequencing in molecular ecology of non-model organisms.
Heredity 107: 1–15.
Etter PD, Preston JL, Bassham S, Cresko WA, Johnson EA. 2011.
Local de novo assembly of RAD paired-end contigs using short
sequencing reads. PLoS ONE 6: e18561.
FAO (Food and Agriculture Organization of the United Nations).
2011. Review of the state of world marine fishery resources.
FAO Fisheries and Aquaculture Technical Paper no. 569.
Rome: FAO.
Farrell ED, Clarke MW, Mariani S. 2009. A simple genetic identi-
fication method for northeast Atlantic smoothhound sharks
(Mustelus spp.). ICES Journal of Marine Science 66: 561–565.
Feldheim KA, Gruber SH, Ashley MV. 2002. The breeding biology
of lemon sharks at a tropical nursery lagoon. Proceedings of the
Royal Society B: Biological Sciences 269: 1655–61.
Feldheim KA, Gruber SH, Ashley MV. 2010. Population genetic
structure of the lemon shark Negaprion brevirostris in the
western Atlantic: DNA microsatellite variation. Molecular Ecology
10: 295–303.
Feldheim KA, Gruber SH, DiBattista JD, Babcock EA, Kessel
SA, Hendry AP, Pikitch EK, Ashley MV, Chapman DD. 2014.
Two decades of genetic profiling yields first evidence of natal
philopatry and long-term fidelity to parturition sites in sharks.
Molecular Ecology 23: 110–117.
Field IC, Meekan MG, Buckworth RC, Bradshaw CJ. 2009.
Susceptibility of sharks, rays and chimaeras to global extinction.
Advances in Marine Biology 56: 275–363.
Filonzi L, Chiesa S, Vaghi M, Marzano FN. 2010. Molecular
barcoding reveals mislabelling of commercial fish products in
Italy. Food Research International 43: 1383–1388.
Fitzpatrick SF. 2012. Global population genetic structure of the
pelagic blue shark (Prionace glauca). PhD thesis, Queen’s
University Belfast, Ireland.
Fowler SL, Cavanagh RD, Camhi M, Burgess GH, Cailliet GM,
Fordham SV, Simpendorfer CA, Musick JA (eds). 2005. Sharks,
rays and chimaeras: the status of the chondrichthyan fishes.
Status survey. Gland: IUCN/SSC Shark Specialist Group.
Geraghty PT, Williamson JE, Macbeth WG, Wintner SP, Harry
AV, Ovenden JR, Gillings MR. 2013. Population expansion and
genetic structure in Carcharhinus brevipinna in the southern
Indo-Pacific. PloS ONE 8: e75169.
Griffiths CL, Robinson TB, Lange L, Mead A. 2010. Marine
biodiversity in South Africa: an evaluation of current states of
knowledge. PloS ONE 5: e12008.
Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Hebert PD.
2006. DNA barcodes distinguish species of tropical Lepidoptera.
Proceedings of the National Academy of Sciences of the USA
103: 968–971.
Hebert PDN, Cywinska A, Ball SL, deWaard JR. 2003. Biological
identifications through DNA barcodes. Proceedings of the Royal
Society B: Biological Sciences 270: 313–321.
Heist EJ, Musick JA, Graves JE. 1996. Mitochondrial DNA diversity
and divergence among sharpnose sharks, Rhizoprionodon
terraenovae, from the Gulf of Mexico and mid-Atlantic Bight.
Fishery Bulletin 94: 664–668.
Helyar SJ, Limborg MT, Bekkevold D, Babbucci M, van Houdt J,
Maes GE, Bargelloni L, Nielsen RO, Taylor MI, Ogden R, Cariani
A, Carvalho GR, FishPopTrace Consortium, Panitz F. 2012.
SNP discovery using next generation transcriptomic sequencing
in Atlantic herring (Clupea harengus). PloS ONE 7: e42089.
Helyar SJ, Lloyd HAD, de Bruyn M, Leake J, Bennett N, Carvalho
GR. 2014. Fish product mislabelling: failings of traceability in
the production chain and implications for illegal, unreported and
unregulated (IUU) fishing. PloS ONE 9: e98691.
Hemmer-Hansen J, Nielsen EEG, Gronkjaer P, Loeschcke V.
2007. Evolutionary mechanisms shaping the genetic population
structure of marine fishes; lessonsfrom the European flounder
(Platichthys flesus L.). Molecular Ecology 16: 3104–3118.
 12
Henriques R, Potts WM, Sauer WHH, Santos CV, Shaw PW.
2014. Incipient genetic isolation of a temperate migratory coastal
sciaenid fish (Argyrosomus inodorus) within the Benguela Cold
Current system. Marine Biology Research 11: 423–429.
Henriques R, Potts WM, Sauer WHH, Shaw PW. 2012. Evidence
of deep genetic divergence between populations of an important
recreational fishery species, Lichia amia L. 1758, around
southern Africa. African Journal of Marine Science 34: 585–591.
Hoelzel AR, Shivji MS, Magnussen J, Francis MP. 2006. Low
worldwide genetic diversity in the basking shark (Cetorhinus
maximus). Biology Letters 2: 639–642.
Holmes BH, Steinke D, Ward RD. 2009. Identification of shark and
ray fins using DNA barcoding. Fisheries Research 95: 280–288.
Hubert N, Hanner R, Holm E, Mandrak NE, Taylor E, Burridge M,
Watkinson D, Dumont P, Curry A, Bentzen P, Zhang J, April
J, Bernatchez L. 2008. Identifying Canadian freshwater fishes
through DNA barcodes. PloS ONE 3: e2490.
Human BA. 2003. Taxonomy and molecular phylogeny of some
southern African catsharks (Scyliorhinidae; Chondrichthyes).
PhD thesis, University of Cape Town, South Africa.
Human BA. 2007. A taxonomic revision of the catshark
Downloaded by [RMIT University] at 07:49 17 August 2015
genus Haploblepharus Garman 1913 (Chondrichthyes:
Carcharhiniformes: Scyliorhinidae). Zootaxa 40: 1–40.
Human BA, Owen P, Compagno LJV, Harley EH. 2006. Testing
morphologically based phylogenetic theories within the
cartilaginous fishes with molecular data, with special reference
to the catshark family (Chondrichthyes; Scyliorhinidae) and the
interrelationships within them. Molecular Phylogenetics and
Evolution 39: 384–391.
Hussey NE, McCarthy ID, Dudley SF, Mann BQ. 2009. Nursery
grounds, movement patterns and growth rates of dusky sharks,
Carcharhinus obscurus: a long-term tag and release study in
South African waters. Marine and Freshwater Research 60:
571–583.
Hutchings L, van der Lingen CD, Shannon LJ, Crawford RJM,
Verheye HMS, Bartholomae CH, van der Plas AK, Louw D,
Kreiner A, Ostrowski M, Fidel Q, Barlow RG, Lamont T, Coetzee
J, Shillington F, Veitch J, Currie JC, Monteiro PMS. 2009. The
Benguela Current: an ecosystem of four components. Progress
in Oceanography 83: 15–32.
IUCN (International Union for Conservation of Nature and Natural
Resources). 2009. IUCN Red List of Threatened Species,
Version 2009.2. Available at http://www.iucnredlist.org [accessed
20 May 2014].
Karl SA. 2008. The effect of multiple paternity on the genetically
effective size of a population. Molecular Ecology 17: 3973–3977.
Karl SA, Castro ALF, Lopez JA, Charvet P, Burgess GH. 2011.
Phylogeography and conservation of the bull shark (Carcharhinus
leucas) inferred from mitochondrial and microsatellite DNA.
Conservation Genetics 12: 371–382.
Keeney DB, Heist EJ. 2006. Worldwide phylogeography of
the blacktip shark (Carcharhinus limbatus) inferred from
mitochondrial DNA reveals isolation of western Atlantic
populations coupled with recent Pacific dispersal. Molecular
Ecology 15: 3669–3679.
Keeney DB, Heupel MR, Hueter RE, Heist EJ. 2005. Microsatellite
and mitochondrial DNA analyses of the genetic structure
of blacktip shark (Carcharhinus limbatus) nurseries in the
northwestern Atlantic, Gulf of Mexico, and Caribbean Sea.
Molecular Ecology 14: 1911–1923.
Kemper JM, Ebert DA, Compagno LJ, Didier DA. 2010. Chimaera
notafricana sp. nov. (Chondrichthyes: Chimaeriformes:
Chimaeridae), a new species of chimaera from southern Africa.
Zootaxa 2532: 55–63.
Krück NC, Innes DI, Ovenden JR. 2013. New SNPs for population
genetic analysis reveal possible cryptic speciation of eastern
Australian sea mullet (Mugil cephalus). Molecular Ecology
Resources 13: 715–725.
Bester-van der Merwe and Gledhill
Lago FC, Vietites JM, Espineira M. 2012. Development of a
FINS-based method for the identification of skates species of
commercial interest. Food Control 24: 38–43.
Lamberth SJ. 2006. White sharks and other chondrichthyan
interactions with the beach-seine (treknet) fishery in False, Bay,
South Africa. African Journal of Marine Science 28: 723–727.
Liu S-YV, Chan C-LC, Lin O, Hu C-S, Chen CA. 2013. DNA
barcoding of shark meats identify species composition and
CITES-listed species from the markets in Taiwan. PLoS ONE 8:
e79373.
Lucifora LO, García VB, Worm B. 2011. Global diversity hotspots
and conservation priorities for sharks. PLoS ONE 6: e19356.
Maduna SN. 2014. Genetic diversity and population genetic
structure in the South African commercially important shark
species, the common smoothhound (Mustelus mustelus). MSc
thesis, Stellenbosch University, South Africa.
Maduna SN, Rossouw C, Roodt-Wilding R, Bester-van der Merwe
AE. 2014. Microsatellite cross-species amplification and utility in
southern African elasmobranchs: a valuable resource for fisheries
management and conservation. BMC Research Notes 7: 352.
Magnussen JE, Pikitch EK, Clarke SC, Nicholson C, Hoelzel AR,
Shivji MS. 2007. Genetic tracking of basking shark products in
international trade. Animal Conservation 10: 199–207.
Marguerat S, Bähler J. 2010. RNA-seq: from technology to biology.
Cellular and Molecular Life Sciences 67: 569–579.
Martin AP, Naylor GJP, Palumbi SR. 1992. Rates of mitochondrial
DNA evolution in sharks are slow compared with mammals.
Nature 357: 153–155.
Melo Palmeira CA, da Silva Rodrigues-Filho LF, de Luna Sales JB,
Vallinoto M, Schneider H, Sampaio I. 2013. Commercialization
of a critically endangered species (largetooth sawfish, Pristis
perotteti) in fish markets of northern Brazil: authenticity by DNA
analysis. Food Control 34: 249–252.
Mendonça FF, Hashimoto DT, Porto-Foresti F, Oliveira C, Gadig
OBF, Foresti F. 2009. Identification of the shark species
Rhizoprionodon lalandii and R. porosus (Elasmobranchii,
Carcharhinidae) by multiplex PCR and PCR-RFLP techniques.
Molecular Ecology Resources 9: 771–773.
Moftah M, Abdel Aziz SH, Elramah S, Favereaux, A. 2011.
Classification of sharks in the Egyptian mediterranean waters
using morphological and DNA barcoding approaches. PLoS
ONE 6: e27001.
Morgan JT, Harry AV, Welch DJ, Street R, White J, Geraghty PT,
Macbeth WG, Tobin A, Simpfendorfer CA, Ovenden JR. 2012.
Detection of interspecies hybridisation in Chondrichthyes:
Hybrids and hybrid offspring between Australian (Carcharhinus
tilstoni) and common (C. limbatus) blacktip shark found in an
Australian fishery. Conservation Genetics 13: 455–463.
Morin PA, Martien KK, Taylor BL. 2009. Assessing statistical power
of SNPs for population structure and conservation studies.
Molecular Ecology Resources 9: 66–73.
Moura T, Silva MC, Figueiredo I. 2015. Barcoding deep-water
chondrichthyans from mainland Portugal. Marine and
Freshwater Research 66: 508–517.
Mourier J, Planes S. 2013. Direct genetic evidence for reproductive
philopatry and associated fine-scale migrations in female
blacktip reef sharks (Carcharhinus melanopterus) in French
Polynesia. Molecular Ecology 22: 201–214.
Musick JA, Burgess G, Cailliet G, Camhi M, Fordham S. 2000.
Management of sharks and their relatives Elasmobranchii.
Fisheries 25: 9–13.
Nance HA, Klimley P, Galván-Magaña F, Martínez-Ortíz J, Marko
PB. 2011. Demographic processes underlying subtle patterns
of population structure in the scalloped hammerhead shark,
Sphyrna lewini. PLoS ONE 6: e21459.
Naylor GJP, Caira JN, Jensen K, Rosana KAM, White WT,
Last PR. 2012. A DNA sequence-based approach to the
identification of shark and ray species and its implications for
 African Zoology 2015: 1–13
global elasmobranch diversity and parasitology. Bulletin of the
American Museum of Natural History 367: 1–262.
Ovenden JR, Berry O, Welch DJ, Buckworth RC, Dichmont CM.
2015. Ocean’s eleven: a critical evaluation of the role of popula-
tion, evolutionary and molecular genetics in the management of
wild fisheries. Fish and Fisheries 16: 125–159.
Ovenden JR, Kashiwagi T, Broderick D, Giles J, Salini JP. 2009.
The extent of population genetic subdivision differs among four
co-distributed shark species in the Indo-Australian archipelago.
BMC Evolutionary Biology 9: 40.
Ovenden JR, Morgan JA, Street R, Tobin A, Simpfendorfer C,
Macbeth W, Welch D. 2011. Negligible evidence for regional
genetic population structure for two shark species Rhizoprionodon
acutus (Rüppell, 1837) and Sphyrna lewini (Griffith & Smith, 1834)
with contrasting biology. Marine Biology 158: 1497–1509.
Peeters FJ, Acheson R, Brummer GJA, De Ruijter WP, Schneider
RR, Ganssen GM, Ufkes E, Kroon D. 2004. Vigorous exchange
between the Indian and Atlantic oceans at the end of the past
five glacial periods. Nature 430: 661–665.
Portnoy DS, Heist EJ. 2012. Molecular markers: progress and
prospects for understanding reproductive ecology in elasmo-
Downloaded by [RMIT University] at 07:49 17 August 2015
branchs. Journal of Fish Biology 80: 1120–1140.
Portnoy DS, McDowell JR, McCandless CT, Musick JA, Graves JE.
2009. Effective size closely approximates the census size in the
heavily exploited western Atlantic population of the sandbar shark,
Carcharhinus plumbeus. Conservation Genetics 10: 1697–1705.
RSA (Republic of South Africa). 1998. Marine Living Resources
Act (Act No. 18 of 1998). Government Gazette, South Africa 395
(18930).
RSA (Republic of South Africa). 2014. National Environmental
Management: Biodiversity Act, 2004 (Act No. 10 of 2004) Draft
Shark Biodiversity Management Plan. Government Gazette,
South Africa 37586.
Schrey AW, Heist EJ. 2003. Microsatellite analysis of population
structure in the shortfin mako (Isurus oxyrinchus). Canadian
Journal of Fisheries and Aquatic Sciences 60: 670–675.
Sembiring A, Pertiwi NPD, Mahardini A, Wulandari R, Kurniasih
EM, Kuncoro AW, Cahyani NKD, Anggoro A, Ulfa M, Madduppa
H, Carpenter KE, Barber PH, Mahardika GN. 2015. DNA
barcoding reveals targeted fisheries for endangered sharks in
Indonesia. Fisheries Research 164: 130–134.
Smale MJ. 2002. Occurrence of Carcharias taurus in nursery areas
of the Eastern and Western Cape, South Africa. Marine and
Freshwater Research 53: 551–556.
Smale MJ, Compagno LJV. 1997. Life history and diet of two
southern African smoothhound sharks, Mustelus mustelus
(Linnaeus, 1758) and Mustelus palumbes Smith, 1957 (Pisces:
Triakidae) South African Journal of Marine Science 18: 229–248.
Smale MJ, Compagno LJV, Human BA. 2002. First megamouth
shark from the western Indian Ocean and South Africa. South
African Journal of Science 98: 349–350.
Sodré D, Rodrigues-Filho LFS, Souza RFC, Rêgo PS, Schneider
H, Sampaio I, Vallinoto M. 2012. Inclusion of South American
samples reveals new population structuring of the blacktip shark
(Carcharhinus limbatus) in the Western Atlantic. Genetics and
Molecular Biology 35: 752–760.
Steinke D, Zemlak TS, Hebert PDN. 2009. Barcoding Nemo:
DNA-based identifications for the ornamental fish trade. PLoS
ONE 4: e6300.
Stevens JD, Bonfil R, Dulvy NK, Walker PA. 2000. The effects of
fishing on sharks, rays, and chimaeras (chondrichthyans), and
the implications for marine ecosystems. ICES Journal of Marine
Science 57: 476–494.
Straube N, Iglésias SP, Sellos DY, Kriwet J, Schliewen UK. 2010.
Molecular phylogeny and node time estimation of bioluminescent
13
lantern sharks (Elasmobranchii: Etmopteridae). Molecular
Phylogenetics and Evolution 56: 905–917.
Teske PR, Zardi GI, McQuaid CD, Nicastro KR. 2013. Two sides of
the same coin: extinctions and originations across the Atlantic/
Indian Ocean boundary as consequences of the same climate
oscillation. Frontiers of Biogeography 5: 48–59.
Tillett BJ, Field IC, Bradshaw CJA, Johnson G, Buckworth
RC, Meekan MG, Ovenden JR. 2012a. Accuracy of species
identification by fisheries observers in a north Australian shark
fishery. Fisheries Research 127: 109–115.
Tillett BJ, Meekan MG, Field IC, Thorburn DC, Ovenden JR.
2012b. Evidence for reproductive philopatry in the bull shark
Carcharhinus leucas. Journal of Fish Biology 80: 2140–2158.
Turner TF, Wares JP, Gold JR. 2002. Genetic effective size is
three orders of magnitude smaller than adult census size in
an abundant, estuarine-dependent marine fish (Sciaenops
ocellatus). Genetics 162: 1329–1339.
Turpie JK, Beckley LE, Katua SM. 2000. Biogeography and the
selection of priority areas for conservation of South African
coastal fishes. Biological Conservation 92: 59–72.
van Sebille E, Biastoch A, van Leeuwen PJ, de Ruijter WPM. 2009.
A weaker Agulhas Current leads to more Agulhas leakage.
Geophysical Research Letters 363: 3.
Velez-Zuazo X, Alfaro-Shigueto J, Mangel J, Papa R, Agnarsson I.
2015. What barcode sequencing reveals about the shark fishery
in Peru. Fisheries Research 161: 34–41.
Walter RP, Kessel ST, Alhasan N, Fisk AT, Heath DD, Chekchak
T, Klaus R, Younis M, Hill G, Jones B, Braun CD, Berumen ML,
DiBattista JD, Priest MA, Hussey NE. 2013. First record of living
Manta alfredi  Manta birostris hybrid. Marine Biodiversity 44: 1–2.
Waples RS. 1998. Separating the wheat from the chaff: patterns
of genetic differentiation in high gene flow species. Journal of
Heredity 89: 438–450.
Ward RD. 2009. Shark fin identification through DNA barcoding.
Endangered Species Update 26: 3–9.
Ward RD, Costa FO, Holmes BH, Steinke D. 2008. DNA barcoding
of shared fish species from the North Atlantic and Australasia:
minimal divergence for most taxa, but Zeus faber and Lepidopus
caudatus each probably constitute two species. Aquatic Biology
3: 71–78.
Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN. 2005. DNA
barcoding Australia’s fish species. Philosophical Transactions of
the Royal Society B: Biological Sciences 360: 1847–1857.
White WT, Last PR. 2006. Description of two new species
of smoothhounds, Mustelus widodoi and M. ravidus
(Carcharhiniformes: Triakidae) from the Western Central Pacific.
Cybium 30: 235–246.
White WT, Last PR. 2008. Description of two new species of
gummy sharks, genus Mustelus (Carcharhiniformes: Triakidae),
from Australian waters. In: Last PR, White WT, Pogonoski JJ
(eds), Descriptions of new Australian chondrichthyans. CSIRO
Marine and Atmospheric Research Paper 022. Canberra:
CSIRO Marine and Atmospheric Research. pp 189–202.
Wong EH-K, Shivji MS, Hanne RH. 2009. Identifying sharks with
DNA barcodes: assessing the utility of a nucleotide diagnostic
approach. Molecular Ecology Resources 9: 243–256.
Worm B, Davis B, Kettemer L, Ward-Paige CA, Chapman D,
Heithaus MR, Kessel ST, Gruber SH. 2013. Global catches,
exploitation rates, and rebuilding options for sharks. Marine Policy
40: 194–204.
Zenger KR, Stow AJ, Peddemors V, Briscoe DA, Harcourt RG.
2006. Widespread utility of highly informative AFLP molecular
markers across divergent shark species. Journal of Heredity 97:
607–611.
Received 28 February 2015, accepted 9 June 2015
Associate Editor: Sandi Willows-Munro