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Morphological Characters of the Thickbody Skate
Amblyraja frerichsi
(Krefft 1968) (Rajiformes: Rajidae),
with Notes on Its Biology
Carlos Bustamante
1,2
*, Julio Lamilla
2
, Francisco Concha
3
, David A. Ebert
4,5,6
, Michael B. Bennett
1
1School of Biomedical Sciences, The University of Queensland, St Lucia, Queensland, Australia, 2Laboratorio de Elasmobranquios (ELASMOLAB), Instituto de Ciencias
Marinas y Limnolo
´gicas, Universidad Austral de Chile, Valdivia, Chile, 3Laboratorio de Biologı
´a y Conservacio
´n de Condrictios, Facultad de Ciencias del Mar y de Recursos
Naturales, Universidad de Valparaı
´so, Chile, Ren
˜aca, Vin
˜a del Mar, Chile, 4Pacific Shark Research Center, Moss Landing Marine Laboratories, Moss Landing, California,
United States of America, 5Research Associate, South African Institute for Aquatic Biodiversity, Grahamstown, South Africa, 6Research Associate, Department of
Ichthyology, California Academy of Sciences, San Francisco, California, United States of America
Abstract
Detailed descriptions of morphological features, morphometrics, neurocranium anatomy, clasper structure and egg case
descriptions are provided for the thickbody skate Amblyraja frerichsi; a rare, deep-water species from Chile, Argentina and
Falkland Islands. The species diagnosis is complemented from new observations and aspects such as colour, size and
distribution are described. Geographic and bathymetric distributional ranges are discussed as relevant features of this
taxons biology. Additionally, the conservation status is assessed including bycatch records from Chilean fisheries.
Citation: Bustamante C, Lamilla J, Concha F, Ebert DA, Bennett MB (2012) Morphological Characters of the Thickbody Skate Amblyraja frerichsi (Krefft 1968)
(Rajiformes: Rajidae), with Notes on Its Biology. PLoS ONE 7(6): e39963. doi:10.1371/journal.pone.0039963
Editor: David Mark Bailey, University of Glasgow, United Kingdom
Received March 13, 2012; Accepted June 1, 2012; Published June 29, 2012
Copyright: ß2012 Bustamante et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This contribution was supported by Direccio
´n de Investigacio
´n of Universidad Austral de Chile (DID-UACH) and Fondo de Investigacio
´n Pesquera (FIP
2006-31/2008-60). The funders had no role in study design data collection and analysis decision to publish or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: c.bustamantediaz@uq.edu.au
Introduction
The genus Amblyraja Malm 1877 (Rajiformes: Rajidae) is a
group of wide-ranging, circumglobal, stout bodied skates that are
found mostly at higher latitudes [1] and in deep tropical waters
[2]; mostly on outer continental shelves, insular shelves and slopes,
and around seamounts [3]. The genus as currently includes ten
nominal species with perhaps two additional undescribed species.
In the south-east Pacific Ocean three poorly known species are
recognized [4]: Amblyraja doellojuradoi (Pozzi 1935), A. frerichsi (Krefft
1968) and A. georgiana (Norman 1938).
Amblyraja doellojuradoi occurs from off Argentina and the Falkland
Islands through the Magellan Strait to off Punta Arenas, Chile at a
reported depth range of 51 to 642 m [5]. Amblyraja georgiana,a
morphologically similar species to A. frerichsi, is an Antarctic species
known from the Antarctic Peninsula [6,7] and South Georgia
Island from a depth range of 150 to about 800 m. Perhaps the
least known species in the region is the thickbody skate A. frerichsi.
Originally described from a type series of 35 subadult and
immature specimens [8] collected between 800 and 1000 m off
the Rio de la Plata, Argentina/Uruguay common fishing zone; this
species has been reported as a rare species in deepwater off Brazil,
Argentina and the Falkland Islands [9211]. Recently, high
bycatch rates of A.frerichsi have been reported from the Magellan
Strait [12]. However, due to a lack of adult descriptive material
and proper field guides, this species largely went unnoticed in
Chile and Argentina deep-sea fisheries. The absence of compar-
ative material and a species-specific description of adults have lead
to unregulated bycatch landings and a lack of capture records due
to misidentification [13], due in part, to a relatively high degree of
variability of morphological characters for this family of elasmo-
branchs [2,3].
Complementary descriptions of the anatomy are usually made
to to clarify the taxonomic status of an important fishery species,
which enabled on-board observers to determine species-specific
landings [14]. Skates worldwide are taken in considerable numbers
either as a directed fishery or indirectly as bycatch [15] and given
that many of skates are landed in large numbers and in a mixture
of species, it is critically important that accurate morphological
descriptions of both adult and subadult fish are available.
The aim of this research is to provide a detailed morphological
description of A. frerichsi from specimens taken as bycatch in
Chilean waters. The neurocranium, clasper, dermal denticles and
egg case morphology are presented as characters to facilitate
identification among other Amblyraja species in the area. New
information on the habitat and fisheries, together with a discussion
of the related conservation implications for this species for the
south-east Pacific are also provided.
Materials and Methods
The specimens used in this study came from historical and
recent bycatch records in the Patagonian toothfish (Dissostichus
eleginoides Smitt 1898) fishery from southern Chile (Figure 1). A
total of 13 males with sizes between 705 to 1201 mm total length
(TL) (mean and standard deviation; 10686163 mm), were caught
between 1989 and 1993, and donated by artisanal fishermen to
ELASMOLAB: two specimens were from off Valdivia (1989), four
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specimens were from Arauco (1990), and seven specimens were
captured between Isla Guamblin and Golfo Ladrilleros (1993). In
addition, 26 females ranging in size from 442 to 1762 mm TL
(9056368 mm) and 26 males ranging between 404 and 1114 mm
TL (8356mm) were caught in the same fishery during 2009
within the research project FIP No. 2008–60, five from off Arauco
and 47 from off Valdivia, and for which sample collection permits
were obtained from the Maritime and Fisheries Authority.
Morphometric measurements and description of key characters
were made in 35 specimens. All measurements were made to the
nearest millimeter (mm), and follow recent recommendations in
the literature [16]. Terminology was adapted from recent
literature for dermal denticles [17], egg capsules [18219], and
clasper [20221] descriptions. The right clasper was removed from
two adult males (1194 mm and 1201 mm TL) and both external
and internal structures are described. The neurocranium was
dissected and described from an adult male (1194 mm TL).
General biological data were also recorded to estimate the size
at maturity, females were considered mature when yellow ovarian
follicles and/or egg capsules were present [22]. Males were
considered mature if sperm were present in their seminal vesicles,
and their claspers were calcified and rigid [23].
Two adult specimens, one male (1094 mm LT) and one female
(1213 mm LT, were preserved and deposited in the Marine Fishes
Collection of Universidad Austral de Chile (Museum accession
number IZUA-PM 4064 and IZUA-PM 4065). Egg capsules were
extracted from a 1445 mm LT female and deposited at
Universidad de Valparaiso Marine Fishes Collection (Museum
accession number CCM-173 and CCM-174).
Results
Amblyraja frerichsi (Krefft 1968).
Thickbody skate (Figures 2, 3, 4, 5, 6, 7, and 8; Tables 1, 2, 3,
and 4).
Synonymy: Raja frerichsi [6,8,24], Raja (Amblyraja) frerichsi [21],
Amblyraja frerichsi [5,25226].
Figure 1. Map of Chile. (A) showing location of study area (inset box),
and collecting localities (B) by date.
doi:10.1371/journal.pone.0039963.g001
Figure 2. Adult male of
Amblyraja frerichsi
(1051 mm TL) in
dorsal (A) and ventral (B) views. Scale bar 100 mm.
doi:10.1371/journal.pone.0039963.g002
Morphology of Amblyraja Frerichsi from Chile
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Diagnosis
A relatively large species of Amblyraja with the following
combination of characters: quadrangular disc, 1.3 times its length
and width 77% TL; tail evenly tapering and robust, width at base
1.3 times first dorsal-fin origin; snout length 23% disc length.
Ventral and dorsal disc uniformly dark-brown to grey-brown
colouration. Dorsal surface densely cover with small dermal
denticles on the head, fins and tail; large hook-shaped denticles on
the orbital series, one preorbital, one postorbital and one
postspiracular; also one nuchal, one scapular and three supra-
scapular are present in the scapular series; and 8226 in the
midline of disc, from behind the scapula to tail. Adult clasper
relatively large, 49% caudal length; and distal lobe extremely
spatulate. Violin-shaped neurocranium with large and bulbous
nasal capsules, with a relatively large rostral shaft ending in a
widened rhomboidal rostral node. Dark brown and finely striated
egg capsules with posterior horns longer than the anterior, both
tapering towards the tips. Horns of egg capsules without lateral
fibrils and coiled terminal tendrils.
Description
Disc quadrangular, 1.28 times as wide as long in adult
specimens, width 77.4% TL, maximum disc width 59.1% TL
(Figure 2). Anterior margin of disc concave behind head, convex at
eye level and concave at spiracle level. Outer margin of disc is
acute angled and posterior margin is slightly convex almost
straight. Snout short, preorbital snout length 0.9 times snout to
spiracle length, 1.9 times interorbital space, 23.7% disc length
(DL). Snout tip pointed, lacking distal process or filament. Orbit
length 2.5 times interorbital space. Spiracle small, 0.9 times orbit
length, 4.9% DL; opening subcircular in shape. Nostril sub-
triangular to oval; anterior nasal flap forms an opening, posterior
lobes not developed meeting medially to form nasal curtain; distal
end sub-rectangular with curved fringe on the posterior margin.
Internarial distance 2.2 times distance between first gill slits,
1.5 times distance between fifth gill slits. Mouth slightly arched in
subadult males and females, curved in adult males; mouth width
1.2 times internarial distance. Teeth with a flat oval base and
acute single cusp, arranged in quincunx without sexual dimor-
phism. Total tooth count in upper jaw 36 (42) arranged in four
rows and in lower jaw 37 (40) arranged in five rows. Bilobed pelvic
fins thin and tapering toward distal end; anterior lobe length 5.7%
DL, with a broad posterior lobe with concave external margin.
Strong tail broad, depressed, tapers from broad base to first dorsal
fin. Tail moderately long, length 43.3% TL; width at insertions of
pelvic fins 1.3 times width at first dorsal-fin origin. Lateral tail fold
long and well developed, length 38% TL, origin after dorsal fins
and extending to tail tip. Dorsal fins strongly acute with long bases
and similar shape. First dorsal fin base length 2.2 times height;
second dorsal fin base length 2.6 times height. Both fin apices
angular; straight posterior inner margins and anterior margins
convex. Dorsal fins sometimes separated by a space, with
interdorsal distance 13% first dorsal-fin base length. Second
dorsal fin continues to a short, undeveloped epichordal caudal
lobe, 0.7 first dorsal-fin base length. Main morphometric
characters expressed as a percentage of total length are found in
Table 2.
Dermal denticles
Dorsal surface with a wide variety of dermal denticles, thornlets
and thorns, but ventral surface with no squamation (Figure 3A).
Small dermal denticles (myrmecoid type), less than 2 mm in height
on subadults and adults, have radial symmetry and cover the
surface of eyelids, pelvic fins and tail, including dorsal and caudal
fins. Basal plate (BP) edge serration of dermal denticles resembles a
426 ridged star (Figure 3B). Thornlets are dermal denticles
usually more than 3 mm height (in subadults and adults), similar in
shape but larger and more robust than dermal denticles. Thornlets
have a small BP with 729 straight furrows and elongated ridges;
Figure 3. Dermal denticles of
Amblyraja frerichsi
.Dorsal view of
the head (A) showing the snout and orbito-spiracular, nuchal and
scapular thorns. Detailed view of malar (B), midline (C), and tail (D)
thorns. (pre) preorbital, (pos) postorbital, (spi) spiracular, (nuc) nuchal,
(sca) scapular, (sup) suprascapular. Scale bar 50 mm (A)or10mm
(B
2
D).
doi:10.1371/journal.pone.0039963.g003
Figure 4. Coloration of
Amblyraja frerichsi
subadult male (985
mm TL) in dorsal (A) and ventral (B) views. Scale bar 100 mm.
doi:10.1371/journal.pone.0039963.g004
Morphology of Amblyraja Frerichsi from Chile
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Figure 5. Neurocranium of
Amblyraja frerichsi
(adult male 1194 mm TL), in dorsal (A), ventral (B), and lateral (C) views. (af) anterior
fontanelle, (bp) basal plate, (eb) epiphyseal bridge, (ecf) ethmoidal canal foramen, (ephf) endolymphatic foramen, (hm VII) hyomandibular branch
foramen, (ja) jugal arches, (nc) nasal capsules, (of) orbital fissure, (pcf) preorbital canal foramen, (pd) parietal depression, (pf) posterior fontanelle, (phf)
perilymphatic foramen, (pof) prootic foramen, (ptc) pteroptic crest, (ptp) pteroptic process, (ra) rostral appendix, (rc) rostral cartilage, (rn) rostral node,
(rs) rostral shaft, (sc) supraorbital crest, (II) optic nerve foramen, (III) oculomotor nerve foramen, (IV) trochlear nerve foramen, (IX) glossopharyngeal
nerve foramen, (X) vagus nerve foramen. Scale bar 50 mm.
doi:10.1371/journal.pone.0039963.g005
Figure 6. General structure of right clasper gland and cartilages of
Amblyraja frerichsi
in lateral. (A) view partially expanded; clasper
cartilages in dorsal (B) and ventral (C) views. (at1) accessory terminal 1, (at2) accessory terminal 2, (ax) axial, (cf) cleft, (dm) dorsal marginal, (dt1) dorsal
terminal 1, (dt2) dorsal terminal 2, (dt3) dorsal terminal 3, (dt4) dorsal terminal 4, (hp) hypopyle, (pe) pent, (ps) pseudosiphon, (rh) rhipidion, (sh)
shield, (sl) slit, (sp) spike, (sr) spur. (st) sentinel, (vm) ventral marginal, (vt) ventral terminal. Scale bar 50 mm.
doi:10.1371/journal.pone.0039963.g006
Morphology of Amblyraja Frerichsi from Chile
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BP with a saddle-like fold and crown curved backward staying
within the BP. Thornlets are densely distributed in rostral and
malar zones beside pectoral fins and parallel, lateral rows in tail.
Additionally, larger denticles that double in size and height
thornlets (usually 60280 mm height in subadults and adults) are
called thorns, and are distributed around head (Figure 3C) and tail
(Figure 3D). The orbital series has three thorns, two in the inner
orbit proximal (preorbital) and distal (postorbital) margins, one
behind spiracle (postspiracular); suprascapular series has one
nuchal, one scapular and three suprascapular thorns, the latter
forming a triangle. In the midline 18226 thorns are present from
the disc, behind the scapula at level of the maximum disc width, to
the tail. Thorns BP have fine radial ridges; wavy-lined lobed edges
in a regular elliptic shape without elongated ridges or furrows.
Thorns acute and curved crown is only one third of BP height and
reaches BP margin. Alar hooks (thorns-like) found only in adult
males in six to eight longitudinal rows near the edge of pectoral
fins. When an interdorsal space is present, one or two thornlets of
variable size present.
Colour
Dorsal disc of fresh adult and subadult male is dark-brown
except blackish-brown distal edges, pelvic fins, tail, dorsal and
caudal fins. Ventral surface uniformly dark-brown (Figure 4).
Dorsal colouration of female is greyish-brown; disc margins,
scapulae and pelvic fins darker. Tail, dorsal and caudal fins are
blackish-brown. In adult males, dorsal and ventral surface is grey-
brown with disc margins, scapulae, pelvic fins, tail and snout a
darker shade. Anterior lobe of pelvic fins, mouth edges, nasal
curtain, cloaca and gill slits are white in all individuals. Sensory
pores clearly visible on the ventral side around the snout and
mouth margins. Sometimes there is a white triangular patch,
where the first two vertices point to the fifth gill slit and the third
vertex to the cloaca. Another oval spot can be seen usually at the
end of the nose. Immature specimen (,400 mm TL) may have
white blotches between gill slits.
Neurocranium
Neurocranium is violin-shaped (Figure 5). Nasal capsules (nc)
are large and bulbous, orientated 70uforward midline rostral
cartilage. Ethmoidal canal foramen (ecf) is located beneath rostral
base, between rostral cartilage (rc) and nasal capsules (nc).
Preorbital canal foramen (pcf) is located in the distal margin of
nasal capsules in the same longitudinal line of the jugal arches (ja).
Strong, angular jugal arches surrounding the parietal fossa (pfs),
with perilymphatic (phf) and endolymphatic (eph) foramina
located in the inner margins. Rostral node (rn) is rhomboidal in
shape with a pronounced concavity at the anterior margin. Rostral
appendices (ra) have two small foramina, the larger with an
inverted triangular-shape. Rostral appendices are c. 37% of rostral
shaft (rs) length. Fontanelles separated by a small epiphyseal
bridge (eb). Anterior fontanelle (af) is oval with a high
resemblance to a blunt arrowhead; while posterior fontanelle
(pf) is ovoid. Posterior fontanelle c. 68% of anterior fontanel
length. Openings of nasal capsules are kidney-shaped with larger
length in same orientation of nasal capsule. The lateral cranial roof
is dorsally limited by the supraorbital crest (sc), with no visible
foramina on surface. Neurocranium basal plate (bp) is short and
narrow at orbit level. Dorsolateral and delimiting the otic capsule,
is located the rounded pterotic process (ptp) which is continuous
towards a low pterotic crest (ptc). Optic nerve foramen (II)is
elliptic and rounded, located in mid-orbital wall. Dorsal to the
Figure 7. Dorsal view of clasper cartilages of
Amblyraja frerichsi
.
Abbreviations of clasper cartilages are indicated at Figure 6. Scale bar
20 mm.
doi:10.1371/journal.pone.0039963.g007
Table 1. Amblyraja frerichsi catches location, sex and depth
by year of historical and recent collections.
Year Depth (m) Sex Geographical position
1993 1,900 4 Male 44u409S; 75u309W
1993 2,200 3 Male 49u019S; 76u209W
1989 1,300 2 Male 39u499S; 74u249W
1990 1,990 4 Male 37u009S; 73u459W
2008 2,200 3 Female 37u579S; 74u129W
2008 2,200 1 Female 38u019S; 74u149W
2008 2,200 1 Female 37u489S; 74u129W
2009 1,280 1 Male 40u089S; 74u179W
2009 1,550 1 Female 40u079S; 74u239W
2009 1,520 1 Male 40u059S; 74u229W
2009 1,253 3 Male; 3 Female 40u069S; 74u239W
2009 1,150 6 Male; 5 Female 40u029S; 74u249W
2009 1,445 1 Male 40u069S; 74u189W
2009 1,317 2 Female 40u069S; 74u179W
2009 1,614 3 Male; 3 Female 40u069S; 74u269W
2009 1,075 1 Male 40u069S; 74u239W
2009 1,037 1 Female 40u109S; 74u189W
2009 1,414 1 Male; 2 Female 40u089S; 74u249W
2009 1,419 1 Male 40u079S; 74u269W
2009 1,729 5 Male: 1 Female 40u059S; 74u239W
2009 1,168 1 Male 39u529S; 74u269W
2009 1,168 1 Male; 1 Female 39u529S; 74u269W
2009 1,168 1 Male; 1 Female 39u509S; 74u229W
2009 1,168 1 Female 39u539S; 74u229W
doi:10.1371/journal.pone.0039963.t001
Morphology of Amblyraja Frerichsi from Chile
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optic nerve foramen are two small openings for the passage of the
trochlear nerve (IV). Posterioventral to the optic nerve foramen is
the foramen for the oculomotor nerve (III). Prootic foramen (pof)
is located in distal margin near orbital fissure (of) and hyoman-
dibular branch of facial nerve foramen (hm VII). The remaining
branches of the trigeminal and facial nerves (V+VII) cannot be
observed at naked eye. Morphometric measurements, expressed in
mm and percentage of nasobasal length are shown in Table 3.
Clasper
Mature males of have moderately long, solid and distally
widened claspers. Clasper length can reach 49% (36250%) of
caudal length in mature males, and all surfaces lack dermal
denticles. In the dorsal surface (Figure 6A), the pseudosiphon (ps)
Table 2. Measurements (mm) of the morphometric
characters taken from 35 specimens of Amblyraja frerichsi.
Morphometric character Min. Max. Mean s.d.
Disc width (DW) 70.77 80.74 77.39 2.54
Disc length (DL) 55.42 59.08 56.73 1.04
Snout length
(preorbital direct) 12 14.78 13.46 0.91
Snout to spiracle 13 15.61 14.32 0.87
Head (dorsal length) 18.37 21.84 19.90 1.02
Eye diameter 2.47 3.16 2.87 0.22
Orbit diameter 2.91 5.07 4.35 0.57
Orbit and spiracle length 4.63 6.38 5.29 0.49
Spiracle length
(main aperture) 2.57 3.27 2.81 0.23
Distance between orbits 6.47 8.04 7.10 0.40
Distance between spiracles 5.83 10.69 8.92 1.20
Snout to cloaca
(1st hemal spine) 50.77 54.96 53.41 1.24
Distance-cloaca to
caudal-fin tip 38.55 43.85 41.41 1.56
Ventral snout length
(pre upper jaw) 10.59 15.49 12.66 1.44
Prenasal length 9.61 12.16 10.88 0.75
Ventral head length
(to fifth gill) 26.3 30.81 29.26 1.29
Mouth width 9.66 12.33 11.23 0.74
Distance between nostrils 8.87 10.56 9.79 0.57
Nasal curtain (total width) 12.8 14.64 13.77 0.64
Width of first gill opening 1.48 2.16 1.76 0.22
Width of fifth gill opening 1.2 2.2 1.63 0.27
Distance between first gill
openings 19.4 23.14 21.16 1.17
Distance between fifth gill
openings 13.66 15.78 14.59 0.74
Length of anterior pelvic lobe 8.34 11.89 9.92 1.07
Tail at axil of pelvic
fins (width) 3.22 4.65 3.88 0.38
Tail at first dorsal-fin
origin (width) 2.5 3.36 2.94 0.28
D1 base length 3.63 4.87 4.35 0.43
D2 base length 3.53 5.69 4.89 0.63
D1 height 1.7 2.44 1.97 0.21
D2 height 1.57 2.13 1.86 0.20
Interdorsal space 0 1.77 0.60 0.56
Caudal-fin length 1.75 3.87 3.15 0.61
Tail lateral folding 35.52 41.93 38.31 1.89
Range expressed as percentage of total length (TL). Mean value (Mean) and
standard deviation (s.d.) are indicated in each case.
doi:10.1371/journal.pone.0039963.t002
Table 3. Measurements (mm) of the neurocranium taken
from one specimen of Amblyraja frerichsi (adult male
1194 mm TL) expressed as percentage of nasobasal length.
mm %
Nasobasal length 128.9 100
Cranial length 225 174.6
Rostral cartilage length 112.5 87.3
Prefontanelle length 71.6 55.5
Cranial width 129.4 100.4
Interorbital width 58.35 45.3
Rostral base 40.4 31.3
Anterior fontanelle length 63.5 49.3
Posterior fontanelle length 20.7 16.1
Anterior fontanelle width 43.2 33.5
Posterior fontanelle width 20 15.5
Rostral cleft length 94.2 73.1
Rostral appendix length 44.8 34.8
Rostral appendix width 32.7 25.4
Posterior foramen of rostral appendix length 33.15 25.7
Cranial height 32.8 25.4
Rostral cartilage height 24.2 18.8
Width across otic capsules 90.5 70.2
Least width of basal plate 38.25 29.7
Greatest width of nasal capsule 50.65 42.2
Internasal width 33.5 26.0
doi:10.1371/journal.pone.0039963.t003
Table 4. Measurements (mm) of the egg capsules of
Amblyraja frerichsi.
CCM-173 CCM-174
Central capsule length 115.5 112.3
Central capsule width 88.5 90.5
Capsule height 15 12.6
Anterior apron length 22.3 17.9
Right anterior horn length 59 59
Left anterior horn length 59 56
Posterior apron length 21.8 20.5
Right posterior outer horn length 54 59
Left posterior outer horn length 53.8 53
Right lateral keel 9.9 10.3
Left lateral keel 13.4 11.6
doi:10.1371/journal.pone.0039963.t004
Morphology of Amblyraja Frerichsi from Chile
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is located in the distal half of clasper and is continued by the cleft
(cf), a narrow longitudinal fissure at same line with the rhipidion
(rh). The slit (sl), a tissue infolding made by the division of axial
cartilage and the proximal end of dorsal terminal cartilage 2, is
located in the proximal half of clasper between ps and cf. In the
outer lateral margin of dorsal lobe and in same line with rh, the
spur (sr) is formed by the distal end of dorsal cartilage terminal 3.
The shield (sh) is an elongated plate located in the internal ventral
lobe, dorsally convex with sharp edges extending from the
hypopyle (hp) up to the pent (pe) and the sentinel (st) on its
distal margin. The rhipidion (rh) is observed as a fan-shaped
protruding structure which extends parallel to the clasper
longitudinal axis and continues to pe, a structure deeply folded
and covered with tissue. In its distal inner margin st is located, a
thick structure, dorsally convex, funnel-like composed by the distal
margin the terminal accessory cartilage 1. The spike (sp) is a small
tab covered by tissue, with the tip pointing towards the dorsal lobe.
The clasper skeleton (Figure 6B) consists of the ellipsoidal axial
cartilage (ax), that flattens dorso-ventrally towards distal margin
where is spatulate; the ax is attached at two-thirds of its length to
the dorsal marginal (dm) and ventral marginal (vm) cartilages. In
the distal margin ax continues to the dorsal terminal cartilage 4
(dt4). Dorsal marginal cartilage (dm) is subrectangular, flattened
and concave, tapering toward distal end and it expands abruptly to
the joint to axial cartilage (Figure 6B27). Dorsal terminal
cartilage 1 (dt1) is long, curved and flattened, with sharp edges
(Figure 7). The small curved t-shaped dorsal terminal cartilage 2
(dt2) is located at dt1 proximal end; while the dorsal terminal
cartilage 3 (dt3), is a flat triangle connected to dt2 in the distal
margin (Figure 6B27). Long, spatulated dorsal terminal carti-
lage 4 (dt4) joins dt3 in the middle dorsal proximal end. Ventral
marginal cartilage (vm) elongated with straight edges, ventrally
curled and acute in the distal end (Figure 6C27). Hook-shaped
ventral terminal cartilage (vt) has a wide-base projection in middle
of the inner edge. Distal half of vt surrounds accessory terminal
cartilage 1 (at1) and is connected to dtr1 distal end. Proximal half
of at1 has an acute, strongly curved appendix (Figure 7), located
below the vmg and connecting to ax. Accessory terminal
cartilage 2 (at2) is small, curved claw-like, located below at1
while proximal end is located under inner edge of vm and at1
junction (Figure 7).
Egg capsules
Capsules in uteri were non-translucent, dorsoventrally flattened
and thick walled. Dark brown coloration in the centre of the
capsule faded to light-brown in the outer margins (Figure 8A).
Surface is finely and longitudinal striated, giving a smooth surface
texture. These striations, hard to distinguish to the naked eye, are
present on the entire capsule surface including horns. In a lateral
view, the dorsal face is convex, while the ventral face is flattened
(Figure 8B). Anterior and posterior margins of the egg capsules are
secured by a thick apron while lateral borders exhibited strong
lateral keels. Anterior apron is concave and against transmitted
light, only the last c. 7 mm of the anterior margin looks
translucent. Posterior apron have a straight posterior margin,
which last c. 10 mm is translucent. Thick and strong lateral keels
were also present the almost full length of the capsule, extending
onto the base of anterior and posterior horns, wider in the middle
of the egg capsules and thinner towards both anterior and
posterior margins. Outer margins of lateral keels are slightly
rounded giving the egg capsules a typical barrel shape. Egg
capsules do not have any lateral or any other accessory adhesion
fibres. Anterior horns are thick, dorsoventrally flattened and
inwardly curved thought not long enough for crossing over. The
inner margin of the horn is united to the anterior apron. The tips
of these horns are fibrous showing a very little coiled end. Posterior
horns are straighter and longer than anterior, and also inwardly
curved on the tips. The inner side of posterior horns are fused with
the posterior apron and became thinner with a tendril-like final
portion. Nevertheless, only the tips are thin and like the anterior
horns, posterior horns have the same terminal entanglement.
Measurements for egg capsules are presented in Table 4.
Size
Specimens examined range in size from 404 to 1762 mm TL.
No individuals with umbilical scars were observed but based on
the egg capsules’ maximum size and the smallest skate specimens
recorded, the size at birth seems to be about 216 mm TL.
Immature specimens range from 216 to 817 mm TL [8]. Adult
females (mature or egg-bearing) ranged from 965 to 1731 mm TL.
Males over 855 mm TL had fully calcified claspers suggesting
maturity is attained between 775 and 907 mm LT. No apparent
sexual dimorphism were observed in size and disc shape.
Distribution
Known distribution on both sides of southern South America,
from Rio de Janeiro, Brazil (22uS) through the Magellan Strait to
Arauco, Chile (37uS). Recorded at depths of 600 to 2,609 m in the
Atlantic Ocean [1,829] and 1,037 to 2,200 m in the Pacific
Ocean.
Discussion
The geographical range of Amblyraja frerichsi, based on verified
records in the literature, extends southwards from Rio de la Plata
(35uS) [8] to the Falkland Islands [10] and Cape Horn (57.3uS)
[12] in the south-west Atlantic; and northwards in the south-east
Pacific, from Cape Horn through the Patagonian Archipelago to
52uS [12]. Our observations extend the latitudinal range in the
south-east Pacific to Arauco (37uS); about 1,700 km north of the
previous confirmed records. It should be noted, however,
unverified records of single specimens have been reported from
Coquimbo (30uS) [27] and the Tarapaca´ Region (23uS) [28] in the
south-east Pacific and Rio de Janeiro, Brazil (22uS) in the south-
Figure 8. Egg capsules of
Amblyraja frerichsi
in dorsal (A) and
lateral (B) views. Scale bar 50 mm.
doi:10.1371/journal.pone.0039963.g008
Morphology of Amblyraja Frerichsi from Chile
PLoS ONE | www.plosone.org 7 June 2012 | Volume 7 | Issue 6 | e39963
west Atlantic. These isolate records may indicate a more extensive
northerly range on each side of South America than is currently
accepted.
No major differences in the anatomy were found when
compared to the original description [8]. However, differences
were found in the spinulation pattern with 16–26 midline thorns
found in comparison to the original description (16–22 thorns [8]).
Colour pattern was also similar to that provided in the original
description, although this character is sensitive to environmental
influences [29] and colour in known to vary in this genus with
immature individuals often darker than adults [30]. No ontoge-
netic growth differences were observed in size and disc shape
between sex and maturity stage.
Internal and external morphology of claspers may help to define
the genus assignment in species specific complex [20,21,31] as has
been documented for deep-water skates, i.e. the Zearaja and
Dipturus complex [32]. Recently, a comprehensive study of the
clasper in three Amblyraja species have been published [33]
contributing to enhance the species diagnosis as a major
component of genus morphology.
Structural consistencies can be detected in the clasper internal
cartilages within A.frerichsi and A. doellojuradoi, A.hyperborea (Collett
1879) and A.radiata (Donovan 1808) [21,33234]; especially in the
shape of the dorsal terminal 2 (dt2) and 4 (dt4); the ventral
terminal and the accessory terminal 1 (at1) and 2 (at2) cartilages.
But the shape and disposition of dorsal terminal 1 (dt1) and 2
(dt2) cartilages are slightly different; and these differences together
may be used in the species diagnosis.
As seen in other skates, the reproductive mode of A. frerichsi is
single oviparity, in which two egg capsules are produced
simultaneously, one in each nidamental gland. Previous descrip-
tions of the egg capsules of Amblyraja species are restricted to a few
species: egg capsules of A. hyperborea and A. robertsi (Hulley 1970) are
bigger than the mean size of those described in this study [35,36];
in contrast to the egg capsules of A. radiata that appear to be
smaller [37]. Nevertheless, all share some common features, such
as colouration pattern, texture, apron thickness and lateral keels.
The absence of accessory lateral adhesion fibres and long non
tendril-like horns are features shared with A.robertsi and A.
hyperborea. Egg capsules of A. radiata have a dense and entangled
bundle of fine adhesion fibres at the top of each anterior horn,
which makes them longer than the posterior horns. In all Amblyraja
egg cases, the posterior horns are longer than the anterior ones,
and taper towards their tips. The general absence of lateral fibrils
or long terminal tendrils suggest that Amblyraja species deposit egg
capsules on the sea floor, rather than attach them to debris or any
other types of substrata.
Amblyraja frerichsi could be potentially confused with other
Amblyraja species present south-east Pacific Ocean because of
similarities in the distribution patterns of dermal denticles and its
general morphology. However, it can be distinguished from A.
doellojuradoi who have white ventral colouration and 12–15 midline
thorns [11,38]. Also it can be differentiated from A.georgiana, who
have large white blotches on the ventral surface and 20–28 midline
thorns [10,38].
An important aspect of this taxon is the geographical and
bathymetric range expansion in the Chilean coast. Capture
records in south Chile (southwards of 40uS) were made at
shallower depths (80021,300 m) than in northern locations
(1,90022,200 m). These depth variations could be evidence of a
relationship between latitudinal ranges, catch depths and water
mass temperature; a hypothesis proposed for Rajella nigerrima (De
Buen 1960) [39] on the continental slope of Chile. The
environmental homogeneity due the Antarctic Intermediate Water
mass that flows at depths of 700 to 1200 m along the Chilean
continental slope [40], may explain the depth range variation
along the latitudinal gradient in the south-east Pacific.
In the south-west Atlantic, capture records of Amblyraja frerichsi
are scarce and restricted to deep waters outside the continental
shelf between 600 and 1,000 m [5,9]. In the same area, off Rio de
la Plata, only immature specimens have been captured predicting
that adults would be at greater depths [8]. In Chile, A.frerichsi
specimens were captured over the continental slope at depths
between 800 and 2,200 m. All female captured shallower than
1,300 m were immature. Sexually mature female were caught at
greatest depths while mature males were observed over the whole
depth range. Such depth-segregation by maturity occurs in a
number of elasmobranch species [41,42]. Spatial and sexual
segregation in A.frerichsi could be related to reproductive events,
such as oviposition [43,44]. Chilean egg-bearing females were
caught in deeper zones as well as deep-water corals (genus
Antipathes and Bathypathes), showing a positive correlation in the
bycatch. Similarly, in the area is thought that the dusky catshark
Bythaelurus canescens (Gu¨nther 1878) use deep-water coral branches
as a substrate for egg-laying [45]. But as other Amblyraja species, A.
frerichsi may deposits its egg capsules on the sea bed and potentially
use the coral gardens as oviposition shelter zones. Tendrils and
curved horns are usually associated with oviposition into complex
three-dimensional substrates, whereas egg cases without tendrils
are generally deposited on bare substrate [45,46]. The reason for
female’s apparent preference for deeper water is uncertain, but
mature female could have a male-avoidance strategy [47] going
deeper to lay her eggs, with young skates migrating to relatively
shallow waters to reduce intraspecific competition [48]. Sex-
specific habitat use has been reported previously for batoid species
[42,43].
Sexual segregation may compromise the integrity of the
population if only mature or immature fraction is caught or
incidentally harvested [49]. A high abundance and bycatch
interaction of A.frerichsi have been reported [12] in the D.
eleginoides fishery around the Patagonian coast of the south-east
Pacific Ocean (52uSto57uS). In this area, A.frerichsi represents
97% of the elasmobranch bycatch by species and 57% of the
elasmobranch biomass caught in this fishery. In the same fishery
but offshore from Valdivia (40uS), have been reported a low
interaction/abundance of A.frerichsi, comprising just 1% of the
total catch [13]. In this fishery while only 8% of the hauls were
made below 1,200 m (between 1,200 and 1,800 m), 65% of the A.
frerichsi catch comprised mature females. The high effort and
pressure made by the fleets in the Patagonian greatly exceeds the
few artisanal vessels that continue catching D.eleginoides [50];
therefore, more immature skates are caught and discarded than
mature fraction maintaining an ephemeral population balance
until bycatch will be evaluated over the entire fisheries distribution
range. The relatively higher abundance in the southern records,
regarding the capture depth range extension, supports the
observation that A.frerichsi prefers cold waters, as do almost all
species of this genus, except A.reversa (Lloyd 1906) who inhabits
deepwater of Arabian Sea [51].
The present study extends the distributional range in the south
Pacific Ocean from 36uS to the Patagonian Channels (54uS), with
a continuous presence along the lower continental slope of Chile.
Besides this geographical extension, the bathymetric distributional
range is also extended, inhabiting between 800 and 2,200 m
depth. It is urgent to focus research in A. frerichsi population sex
and maturity structure, especially in the area where it occurs as
bycatch in the Patagonian toothfish (D.eleginoides) fishery from the
Morphology of Amblyraja Frerichsi from Chile
PLoS ONE | www.plosone.org 8 June 2012 | Volume 7 | Issue 6 | e39963
southern channels of Chile, where overfishing could threaten the
integrity and balance of this skate’s population.
Acknowledgments
Authors wish to thank all members of the ELASMOLAB involved in
‘‘Programa de Conservacio´n de Tiburones (PCT)’’, for their valuable help
with logistics, sampling and dissections. We are very grateful to fishermen
involved, especially to the ‘‘L/M Pamela II’’ crew and L. Ferna´ ndez for his
valuable help in field. Additional thanks to S. Sa´ ez, C. Sepu´ lveda, E.
Acun˜a, M. Vargas, M. Stehmann and U. Gomes for their suggestions and
comments in an early versions of this article; to J. Pollerspo¨ ck (Shark-
References.com) for providing literature. Thanks to the academic editor
and two anonymous reviewers for their comments in the final stage of this
manuscript.
Author Contributions
Conceived and designed the experiments: CB JL. Performed the
experiments: CB FC. Analyzed the data: CB DAE MBB. Contributed
reagents/materials/analysis tools: JL. Wrote the paper: CB FC DAE MBB.
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