Upeneus nigromarginatus, a new species of goatfish (Perciformes: Mullidae) from the Philippines

Abstract

The goatfish, Upeneus nigromarginatus new species, is described based on 5 specimens (151–196 mm) purchased at a fish market in Panabo City, Mindanao, Philippines. This species is diagnosed by the following counts and external morphology: dorsal fin rays (VIII, 9–10), pectoral fin rays (16), lateral line scales (36–37), total number of gill rakers (25–26), and anal fin rays (I–II, 6). When compared to congeners, U. nigromarginatus new species has a relatively deeper body (31.1–34.8% in SL vs. <30% in SL), shorter snout (7.1–9.0% in SL vs. >9.6 % in SL), and longer pectoral fin (27.7–29.1% in SL vs. <25 % in SL). Upeneus. nigromarginatus new species, has neither stripes on the body, nor bands on the caudal fin. However, a black band borders the distal edges of both the first and second dorsal fins, and at the posterior edge of the upper lobe of the caudal fin; hence the proposed common name ‘black-margined goatfish’. The posterior edge of the ventral caudal lobe has a white margin. The comparisons of a fragment of the Cytochrome C Oxidase Subunit I (COI; 28 specimens representing 10 Upeneus species) and 34 morphometric parameters (Principle Component Analysis; 56 specimens representing 5 genera and 12 mullid species) supported the description of U. nigromarginatus new species.

Full text

750
Bos: New species of goatsh from the Philippines
Upeneus nigromarginatus, a new species of goatfish (Perciformes:
Mullidae) from the Philippines
Arthur R. Bos1, 2, 3
Abstract. The goatsh, Upeneus nigromarginatus, new species, is described based on ve specimens (151–196
mm) purchased at a sh market in Panabo City, Mindanao, Philippines. This species is diagnosed by the following
counts and external morphology: dorsal n rays (VIII, 9–10), pectoral n rays (16), lateral line scales (36–37), total
number of gill rakers (25–26), and anal n rays (I–II, 6). When compared to congeners, U. nigromarginatus, new
species has a relatively deeper body (31.1–34.8% in SL vs <30% in SL), shorter snout (7.1–9.0% in SL vs >9.6% in
SL), and longer pectoral n (27.7–29.1% in SL vs <25% in SL). Upeneus nigromarginatus, new species, has neither
stripes on the body, nor bands on the caudal n. However, a black band borders the distal edges of both the rst
and second dorsal ns, and at the posterior edge of the upper lobe of the caudal n; hence the proposed common
name ‘black-margined goatsh’. The posterior edge of the ventral caudal lobe has a white margin. The comparisons
of a fragment of the cytochrome C oxidase subunit I (COI; 28 specimens representing 10 Upeneus species) and
34 morphometric parameters (Principle Component Analysis; 56 specimens representing ve genera and 12 mullid
species) supported the description of U. nigromarginatus, new species.
Key words. COI, Coral Triangle, Mulloidichthys, Mullus, Parupeneus
RAFFLES BULLETIN OF ZOOLOGY 62: 750–758
Date of publication: 1 December 2014
http://zoobank.org/urn:lsid:zoobank.org:pub:2B16517F-3948-4EBC-A90F-2E49BC5E6F37
© National University of Singapore
ISSN 2345-7600 (electronic) | ISSN 0217-2445 (print)
1Department of Biology, School of Sciences and Engineering, The American University
in Cairo, P.O. Box 74, New Cairo 11835, Egypt; Email: arthurrbos@yahoo.com; Tel:
+20 2 2615 2903
2Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, the Netherlands
3Davao del Norte State College, New Visayas, 8105 Panabo, the Philippines
Taxonomy & Systematics
INTRODUCTION
Representatives of the goatfish family Mullidae are
recognised by an elongate body with two separate dorsal
ns and two unbranched barbels on the chin. This family
consists of six genera with 83 species worldwide. In the
western Pacic Ocean, this family is represented by the
genera Mulloidichthys, Parupeneus and Upeneus with 41
recognised species (Froese & Pauly, 2014). These genera can
be differentiated based on the number of lateral line scales
and the distance between the two dorsal ns: Mulloidichthys
has 33–39 lateral line scales and 5 inter-dorsal n scale
rows, Parupeneus 26–31 lateral line scales and 3 inter-dorsal
n scale rows, and Upeneus 28–39 lateral line scales and
5–7 inter-dorsal n scale rows (Randall, 2001; Uiblein &
Heemstra, 2010). The presence and shape of teeth allow
further generic discrimination (Randall, 2001). Parupeneus
and Mulloidichthys lack teeth on the vomer and palatine.
Teeth on oral jaws are conical in Parupeneus while villiform
in the other two genera.
The genus Upeneus consists of 30 species worldwide, of
which 11 species have been recorded in the Philippines
(Froese & Pauly, 2014). Uiblein & Heemstra (2010)
recognised four Upeneus species groups that include 25
of the 26 Indo-Pacic species. These groups are based on
clustered combinations of the number of dorsal spines (VII
or VIII), total number of gill rakers (18–33), the number of
pectoral n rays (13–17), and the presence/absence of bars
on the caudal n.
The present study is based on several goatsh specimens
purchased at the Panabo City market near the northern coast
of the Davao Gulf, a large bay in southeast Mindanao, the
Philippines (Fig. 1). The species could not be identied
using existing taxonomic keys and literature. External
morphological characters, morphometric and genetic
comparisons with other mullids supported the description
of Upeneus nigromarginatus, new species, as presented in
this manuscript.
MATERIAL AND METHODS
Morphological analysis. Five specimens were purchased at
a market in Panabo City, the Philippines (see Fig. 1 in Bos
et al., 2011a) on 26 June 2012. Specimens were measured
after preservation in ethanol at the Naturalis Biodiversity
Center in Leiden, the Netherlands in January 2014. Metric
data, including counts of all n rays and the scales along
the lateral line were collected (Table 1). Gill rakers were
counted on the first gill arch separating those from the
upper and lower limbs (Table 1). Furthermore, gill rakers
were categorised ‘developed’ (length-width ratio ≥1) or
‘undeveloped’ (length-width ratio <1). Morphological traits
(Table 2) were adapted from Randall & Kulbicki (2006) and
Uiblein & Heemstra (2010). Measurements were done with

751
RAFFLES BULLETIN OF ZOOLOGY 2014
Table 1. Meristic data of the holotype, paratypes (n = 4), and mode of all specimens (n = 5) of Upeneus nigromarginatus, new species.
Meristic characteristic Holotype Paratypes Mode
Rays in rst dorsal n VIII VIII VIII
Rays in second dorsal n 9 9–10 9
Rays in anal n I,6 I,6–II,6 II,6
Rays in pelvic n I,5 I,5 I,5
Rays in pectoral n 16 16 16
Rays in caudal n 15 15–16 15
Lateral line scales 36 36–37 36
Gill rakers (upper limb, undeveloped) 3 2–3 3
Gill rakers (upper limb, developed) 5 4–6 5
Gill rakers (lower limb, developed) 13 12–13 13
Gill rakers (lower limb, undeveloped) 4 5–6 5
Total gill rakers on upper limb 8 7–9 8
Total gill rakers on lower limb 17 17–18 18
Total gill rakers 25 25–26 25
Fig. 1. Map of the Philippines archipelago with Davao Gulf in the
South-East of Mindanao Island.
a vernier caliper at 1 mm accuracy for measures >10 mm
and at 0.1 mm accuracy for measures ≤10 mm.
All type specimens were deposited in the Naturalis
Biodiversity Center (former Rijksmuseum voor Natuurlijke
Historie; RMNH) in Leiden, the Netherlands. For comparison,
representative species of the western Pacific genera of
the Mullidae (Mulloidichthys, Parupeneus, Upeneus)
were selected from the collections of RMNH and the
Zoological Museum in Amsterdam (ZMA; presently stored
at the RMNH). Some specimens of the genera Mullus and
Pseudupeneus were included to increase the accuracy of
the analysis. Similar-sized shes were selected, if available,
to avoid effects of ontogenetic changes on measured ratios
(Standard Length [SL] between 140 and 230 mm).
Molecular analysis. A gill arch was removed from all ve
type specimens, immediately preserved in 96% ethanol
and stored in a freezer (at −80°C). For method verication,
gill tissue of three other goatshes was also collected in
the Philippines in June 2012: one sample of Parupeneus
barberinus (Lacepède, 1801), one sample of Parupeneus
indicus (Shaw, 1803) and one sample of Upeneus tragula
Richardson, 1846.
Genetic material was extracted from 25–50 mg of tissue
with a proteinase K digestion using a QIA-amp DNA
mini-kit protocol (QIAGEN). For DNA amplication and
sequencing, a standard 25 µl Polymerase Chain Reaction
(PCR) mix was used containing 5 µl of 5× PCR buffer,
0.75 µl dNTP, 0.25 µl Taq Polymerase, 1 µl of each primer
(forward and reverse), 1.5 µl MgCl2, 2 µl DNA template, and
13.5 µl H2O. The following primers were used: FishF1- 5’
TCAACCAACCACAAAGACATTGGCAC and FishR1-5’
TAGACTTCTGGGTGGCCAAAGAATCA (Steinke &
Hanner, 2010). A 655 base pair (bp) region of Cytochrome
C Oxidase Subunit I (COI) was subsequently amplied
under the following conditions: 5 min at 95°C; 35 cycles
of 30 s at 95°C, 45 s at 45°C, and 60 s at 72°C; 7 min at
72°C; held at 4°C.
Data analysis. Principle Component Analysis (PCA) was
conducted to visualise metric differences between the
proportional morphologic measures (percentage of SL) with
the highest variation of all studied specimens. Direct Oblimin
Rotation with Kaiser Normalization (SPSS Statistics 20)
was used to nd the rotated components with the highest
signicance.
Nucleotide sequences (COI) of similar length (about 655
bp) were used to conduct the genetic comparison (GenBank,
2014). All Upeneus species, for which COI sequences were
uploaded to GenBank, were included in the analysis (Table

752
Bos: New species of goatsh from the Philippines
Table 2. Proportional morphological measurements of the holotype, paratypes (n = 4), and mean for all specimens (n = 5) of Upeneus
nigromarginatus, new species, as percentages of standard length (SL).
Holotype Paratypes Mean
Standard Length (mm) 196 151–156 162.6
Measurement % SL % SL % SL
Body depth at D1 34.7 31.1–34.8 32.9
Half body depth at D1 26.0 23.8–26.5 25.0
Body depth at A 28.6 27.1–30.3 28.4
Half body depth at A 20.4 19.2–20.6 20.0
Caudal peduncle depth 12.8 12.6–12.9 12.8
Jaw depth 12.8 11.9–12.3 12.3
Head depth through eye 21.9 21.3–23.2 22.4
Head length 29.1 29.1–30.3 29.8
Jaw length 11.2 11.3–12.3 11.7
Barbel length 19.9 20.5–20.6 20.4
Snout length 8.7 7.1–9.0 8.3
Orbit diameter 7.1 7.7–9.0 8.2
Pre dorsal length 36.2 35.5–37.2 36.2
D1 base length 15.3 14.7–15.9 15.1
D1 n height 24.5 24.5–25.2 24.7
Inter dorsal length 15.3 14.6–16.1 15.4
D2 base length 13.8 14.6–17.4 15.2
D2 n height 16.8 17.4–18.7 17.8
Pre pectoral length 30.6 31.6–34.0 32.2
Pectoral n length 28.6 27.7–29.1 28.7
Pre pelvic length 33.2 32.9–35.1 33.7
Pelvic n length 19.9 20.0–21.8 20.6
Pre anal length 70.9 68.4–71.8 70.3
Anal base length 10.2 10.3–11.0 10.6
Anal n height 15.8 16.1–16.7 16.3
Caudal peduncle length 18.4 17.9–21.9 19.5
Caudal n length 28.6 27.7–31.4 29.2
Caudal concavity 15.3 12.9–16.1 14.3
Body width 16.3 16.0–17.2 16.4
Inter orbit width 8.7 7.7–8.6 8.3
Nostril width 5.1 5.8–6.0 5.7
3). If available, three specimens per species were selected
to increase genetic diversity among conspecics. Specimens
of the genus Parupeneus were selected as outgroup taxa.
Sequence alignment (MUSCLE; 20 renement iterations)
and phylogeny reconstruction (Maximum Likelihood under
the General Time Reversible substitution model; Gamma
distributed with Invariant site; Nearest-Neighbor-Interchange;
and maximum parsimony with 500 replicates bootstrap
analysis) were conducted with the software package MEGA
5.10. Bootstrap values ≤50% at the nodes of the clades did
not allow exact reconstruction of the phylogenetic history
of the Upeneus species and are not shown.
RESULTS
Morphological comparison. The PCA resulted in four
principle components respectively explaining 29.3, 16.2,
12.7 and 6.2% of the variance in the data matrix (Fig. 2).
Component 1 explained variance of (listed by decreasing
importance) jaw depth, head depth through eye, D2 base
length, anal base length, pelvic n length, body depth at A,
half body depth at D1, half body depth at A, body depth
at D1, number of scales, snout length, barbel length, inter
dorsal length, pectoral n length. Component 2 explained
variance of pre-pelvic length, pre-anal length, D1 height,
caudal peduncle length, pre-dorsal length, orbit diameter
and pre-pectoral length. The five represented genera
Mulloidichthys, Mullus, Parupeneus, Pseudupeneus, and
Upeneus occupied unique regions within the rotated axes
(Fig. 2). Species of Parupeneus and Pseudupeneus, and
those of Mullus and Upeneus partly overlapped, whereas
the specimens representing Mulloidichthys were relatively
isolated. The ve specimens of Upeneus nigromarginatus,
new species, formed a completely isolated cluster (Fig. 2),
positioned nearest to specimens of Mullus and Upeneus.

753
RAFFLES BULLETIN OF ZOOLOGY 2014
TAXONOMY
Upeneus nigromarginatus, new species
Black-margined goatsh
(Figs. 3–5; Tables 1, 2)
Material examined. Holotype (Fig. 3): RMNH.PISC.37991, 1 ex.,
196 mm SL; The Philippines, Panabo City, sh market, 7°18ʹ23ʺN,
125°41ʹ1ʺE, coll. A.R. Bos, 26 June 2012. Paratypes: RMNH.
PISC.36422, 1 ex., 151 mm SL; RMNH.PISC.36423, 1 ex., 155 mm
Fig. 2. Principle Component Analysis of 34 morphological
parameters of 56 specimens representing the Mullidae. Species
clusters are shown for ve genera (Mulloidichthys avolineatus
[black square], Mulloidichthys martinicus [crossed square],
Mulloidichthys vanicolensis [open square], Mullus auratus [black
triangle], Mullus surmuletus [open triangle], Parupeneus barberinus
[black inverted triangle], Parupeneus heptacanthus [open inverted
triangle], Parupeneus indicus [open inverted triangle with dot],
Pseudupeneus maculatus [open diamond], Pseudupeneus prayensis
[half-lled diamond], Upeneus nigromarginatus, new species [star],
Upeneus tragula [black circle], Upeneus vittatus [open circle]).
Fig. 3. A, Upeneus nigromarginatus, new species, holotype,
RMNH.PISC.37991, fresh specimen; B, holotype after 4 months
in ethanol, SL 196 mm.
Table 3. GenBank Accession numbers of goatsh specimens (Mullidae) with taxonomic author used in the phylogenetic analysis.
Species Author Accession number
Parupeneus barberinus (Lacepède, 1801) JQ3501791, JQ3501801
Parupeneus indicus (Shaw, 1803) DQ8850372, FJ2378832
Upeneus japonicus (Houttuyn, 1782) EF6076033, EF6076043, JF9528844
Upeneus margarethae Uiblein & Heemstra, 2010 KC1478012, KC1478052, KC1477982
Upeneus mascareinsis Fourmanoir & Guézé, 1967 KC1478072
Upeneus moluccensis (Bleeker, 1855) KC5018335, KC5018515, KC5018525
Upeneus parvus Poey, 1852 JQ3656136, JQ3656156, KF9305192
Upeneus pori Ben-Tuvia & Golani, 1989 KF5643192
Upeneus sulphureus Cuvier, 1829 EF6076093, EF6096357, EF6096367
Upeneus tragula Richardson, 1846 EF6076123, KC1477992
Upeneus vittatus (Forskåll, 1775) FJ2375387, GU8049722, JX6761552
1(Hubert et al., 2012); 2 unpulished data; 3(Zhang, 2011); 4(Zhang & Hanner, 2011); 5(Keskin & Atar, 2013); 6
(Oliveira Ribeiro et al.,
2012); 7(Lakra et al., 2011)
SL; RMNH.PISC.36424, 1 ex., 156 mm SL; RMNH.PISC.37992,
1 ex., 155 mm SL, same collection information as holotype.
Diagnosis. Meristic data of the holotype and the range and/or
median of all type specimens are provided in Table 1. Data
in parentheses refer to the paratypes when different from the
holotype. Dorsal n VIII + 9, rst dorsal spine small, second
dorsal spine longest, last dorsal soft ray branched to base.
Anal n I, 6, three paratypes with unusual two spines instead
of one, with rst spine short and thin (Fig. 4), second spine
up to two-third of rst soft ray, rst anal soft ray segmented
and unbranched, last ray branched to base. Pectoral n rays
16, upper 2 rays unbranched. Pelvic n rays I, 5. Principal
caudal n rays 15 (15–16), uppermost and lowermost rays
unbranched. Lateral line scales 36 (36–37), ve scale rows
between dorsal ns. Total gill rakers on rst gill arch 25
(25–26). Gill rakers on upper and lower limb of rst arch

754
Bos: New species of goatsh from the Philippines
Fig. 4. Upeneus nigromarginatus, new species, paratype, RMNH.
PISC.36423, anal n with two spines and six soft rays. White arrow
points at short, thin rst spine.
8 + 17 (7–9 + 17–18), several anterior rakers undeveloped
but visible on both limbs.
Proportional measurements of the holotype, paratypes, and
the mean value of all specimens are presented in Table 2.
Body relatively deep, its depth at rst dorsal n origin 2.9
(2.9–3.2) in SL. Body width 2.1 (1.8–2.2) in body depth.
Anterior dorsal n height 4.1 (4.0–4.1) in SL. Head length
(HL) 3.4 (3.3–3.4) in SL. Snout relatively short, its length
3.4 (3.4–4.3) in HL. Orbit diameter 4.1 (3.6–3.9) in HL.
Nostrils at horizontal axis of ventral edge of orbit. Mouth
terminal and slightly oblique, the cleft forming an angle of
about 10° to the horizontal axis of body. Both jaws with
several rows of unevenly placed villiform teeth. Palatine
and vomer with villiform teeth. Vomer with smaller teeth
than those on palatine, forming rough surface covered by
membrane tissue. Maxilla reaching vertical through anterior
half of pupil, upper jaw length 2.3 (2.4–2.5) in HL. Barbels
reaching vertical at two third of distance between orbit
and posterior margin of pre-operculum, their length 1.5
(1.4–1.5) in HL.
Origin of dorsal n over fth lateral-line scale, pre-dorsal
length 2.8 (2.7–2.8) in SL. Longest dorsal spine 1.2 in HL.
First dorsal spine very short; pectoral n relatively long, its
length 1.0 (1.0–1.1) in HL. Pelvic n length 1.5 (1.4–1.5) in
HL. Caudal n length relatively short, its length 1.0 (1.0–1.1)
in HL. Caudal n moderately forked, caudal concavity 1.9
(1.9–2.4) in HL. Caudal peduncle depth 2.3 (2.3–2.4) in HL.
Caudal peduncle length 1.6 (1.4–1.7) in HL. Pre-anal length
1.4 (1.4–1.5) in SL. Anal n height 1.8 (1.8–1.9) in HL.
Scales nely ctenoid. Sensory canals on lateral-line scales
with four to six branches. A row of about 17 sensory canals
on posterior edge of pre-operculum. Opercular membrane
forms pointed lobe at horizontal axis of mid-eye position,
but lacks a spine. Cheek and pre-operculum covered with
scales. Small scales present basally on posterior dorsal and
anal n. Slender pelvic axillary scale about half the length
of the pelvic n.
Coloration in life. Coloration based on the freshly dead
specimen of the holotype (Fig. 3A). Body and abdomen
pearly white without conspicuous stripes or bands. Snout red,
color continuing until pre-operculum. Nape reddish. Silver
white line at an angle of about 20° to the horizontal axis of
body from nostril to eye, line continues along margin of the
orbit decreasing in width posteriorly. Scales above lateral line
on body with red margins, but less conspicuous on caudal
peduncle. Barbels white with rosy tips. Inter-radial tissue of
D1 red between 2nd and 3rd rays, translucent between other
rays (Fig. 5A). Second dorsal n translucent with scattered
reddish blotches (Fig. 5B). Distal endings of D1 and D2
with a thin black margin, some specimens with a thin white
line or few white blotches proximal to the black margin in
the anterior dorsal n. Caudal n reddish with increasing
intensity towards n tips (Fig. 5C). Posterior end of dorsal
lobe of caudal n with a black margin, terminating slightly
ventral to the caudal fork. Ventral lobe of caudal n has a
bright white margin at its proximal end, which increases in
width towards the tip of the lobe. A brownish blotch or line
anterior to the white margin on the ventral lobe of caudal
n (Fig. 5C). Anal n white with a translucent sphere in its
center. Pectoral ns translucent. Small red blotches just dorsal
of pectoral n bases. Pelvic ns translucent with white tips.
Coloration in preserved specimens. Coloration of the
holotype after preservation in ethanol is shown in Figure 3B.
Area dorsal to lateral line pale white; ventral to lateral line
red-purplish. All ns pale white, with black margins along
anterior dorsal n, posterior dorsal n, and upper lobe of
caudal n. Silver-white line from nostril to eye.
Distribution. This species is only known from the northern
region of the Davao Gulf in the Philippines (Fig. 1).
Etymology. The name of this species derives from the black
margins along both dorsal ns and the dorsal lobe of the
caudal n.
Fig. 5. Selected ns of fresh specimen of Upeneus nigromarginatus,
new species, holotype, RMNH PISC.37991 (not to scale); A, anterior
dorsal n; B, posterior dorsal n; C, caudal n.

755
RAFFLES BULLETIN OF ZOOLOGY 2014
Remarks. The black-margined goatfish Upeneus
nigromarginatus, new species, differs from other Upeneus
species (Table 2) in having a deeper body (31.1–34.8% in SL
at origin of rst dorsal n), longer pectoral ns (27.7–29.1%
in SL), and a shorter snout (7.1–9.0% in SL). Uiblein &
Heemstra (2011) compared seven Upeneus species and
found body depth at the rst dorsal n never to exceed 30%
in SL. The longest pectoral n (25% in SL) was found in
Upeneus francisi and the shortest snout (9.6% in SL) was
recorded for Upeneus guttatus (Uiblein & Heemstra, 2011).
Several of the type specimens of U. nigromarginatus, new
species, have two spines in the anal n (Fig. 4), although one
anal spine is diagnostic for Upeneus (Uiblein & Heemstra,
2011). All other characteristics justied the classication
of the new species to the genus of Upeneus. The presence
of palatine and vomerine teeth is diagnostic for Upeneus
(Uiblein & Heemstra, 2011). Upeneus nigromarginatus, new
species, has villiform teeth on the palate and the vomer,
but teeth are smaller in size on the latter. Some individuals
of Upeneus lifer, completely lack vomerine teeth (Kim,
2002) and therefore the smaller size of vomerine teeth was
not considered a feature supporting separation from the
Upeneus genus.
Ecological information. Specimens of Upeneus
nigromarginatus, new species, were sold in a market in
Panabo City by a vendor, who introduced me to the sherman
who caught the fish. An interview with the fisherman
revealed that these shes were caught with a gill net (mesh
size 2 inches) at a depth of 40–80 m approximately at the
coordinates 7°14ʹ32ʺN, 125°40ʹ17ʺE. The net was set at
0400 h of 26 June 2012 and then retrieved an hour later.
Upeneus nigromarginatus, new species, was caught together
with Upeneus vittatus (Forsskål, 1775), Polydactylus
longipes Motomura, Okamoto, Iwatsuki, 2001, and Rexea
bengalensis Alcock, 1894. Upeneus nigromarginatus, new
species, is a relatively uncommon species, evidenced by the
few individuals which have been caught by shermen living
along the shores of the Lasang River estuary. Anecdotal
evidence suggested that shermen from the northern villages
in Samal Island (Davao Gulf) may have caught specimens of
this species (pers. comm. N. Gallarda), but a 2-year survey
conducted at local sh markets in Samal Island did not
reveal other specimens of U. nigromarginatus, new species
(Bos & Gumanao, 2012).
Genetic comparison. The COI fragments of 34 goatshes
provided, after alignment and trimming to equal length, 581
nucleotides for analysis with 208 variable characters. The
phylogenetic tree resulting from the Maximum Likelihood
construction is shown in Fig. 6. All specimens formed
monophyletic sub-clades with their conspecifics with
bootstrap values of ≥74% with only Parupeneus barberinus
showing a lower bootstrap value. The ve specimens of U.
nigromarginatus, new species, were positioned within the
monophyletic clade of Upeneus and formed a sub-clade with
a bootstrap value of 97%.
A second sub-clade consisted of 10 specimens representing
U. japonicus, U. margarethae, U. pori, and U. tragula was
well supported with a bootstrap value of 77%. A third sub-
clade included 10 specimens representing U. mascareinsis,
U. moluccensis, U. sulphureus, and U. vittatus was supported
with a bootstrap value of 57%. Three specimens representing
U. parvus formed a fourth sub-clade with a bootstrap value
of 99%.
DISCUSSION
Four taxa groups are recognised for 25 species of the genus
Upeneus in the Indo-Pacic based on a combination of
morphological characters: the number of dorsal n spines
(D1), pectoral n rays (PFR), gill rakers (GR), and bars
on the caudal n (Uiblein & Heemstra, 2010). These four
groups are; “japonicus group” (seven species: D1 VII, PFR
13–15, GR 21–32, bars present ), “tragula group” (seven
species: D1 VIII, PFR 13–14, GR 18–25, bars present),
“moluccensis group” (four species: D1 VIII, PFR 15–17,
GR 26–33, bars mostly absent), and “vittatus group” (seven
species: D1 VIII, PFR 15–17, GR 26–32, bars present). Only
one species occurring in the area, Upeneus lifer Ogilby,
1910, does not t into these categories based on a unique
combination of the above meristic data (D1 VIII, PFR 13–14,
GR 24–27) and absence of bars on the caudal n (Uiblein
& Heemstra, 2010).
Based on its eight dorsal n rays and the relatively low total
number of gill rakers (25–26), Upeneus nigromarginatus, new
species, could be added to the “tragula group”. However,
representatives of the “tragula group” are further recognised
in having 13–14 pectoral n rays and bars on the caudal
n. In contrast, U. nigromarginatus, new species, has 16
pectoral fin rays and does not have bars on the caudal
n. The caudal n coloration of U. nigromarginatus, new
species, is comparable to that of two representatives of the
“moluccensis group”; Upeneus doriae Günther, 1869 and
Upeneus sulphureus Cuvier, 1829 (Uiblein & Heemstra,
2010), but these respectively have 29–33 and 27–28 gill
rakers. Therefore, U. nigromarginatus, new species, shares
characteristics with representatives of more than one of the
species groups and cannot be clearly categorised, as is the
case with Upeneus lifer. However, the present COI analysis
provided support for the species groups (Fig. 6). The two
monophyletic sub-clades representing multiple Upeneus
species exactly differentiated between “moluccensis” and
“vittatus” representatives and “japonicus” and “tragula”
representatives (Uiblein & Heemstra, 2010).
Phylogenetic relationships of the goatfishes have been
studied, but were usually limited to relatively few species.
Mamuris et al. (1999) found the genus Pseudupeneus being
most genetically distinct from those of Mullus and Upeneus,
which is congruent to the present morphological comparison
(Fig. 2). Lakra et al. (2011) recovered three separate clades
for the genera Parupeneus, Mulloidichthys, and Upeneus. As
these earlier studies included only three species (Upeneus
moluccensis, U. sulphureus, and U. vittatus), the present
study with 10 representative species, comprises the most
comprehensive COI comparison for the Upeneus genus.

756
Bos: New species of goatsh from the Philippines
Fig. 6. Maximum likelihood phylogeny of representatives of the genus Upeneus (Mullidae). Species names are accompanied by GenBank
association numbers, except for those specimens analysed during the ‘present study’ (method validation) and specimens of Upeneus
nigromarginatus, new species (RMNH collection numbers). Representatives of the genus Parupeneus were used as an outgroup. Numbers
at nodes represent maximum parsimony bootstrap proportions.
The Davao Gulf, located in the South East of the Philippines,
is geographically isolated and has faunal elements differing
from other parts of the archipelago as it is dominated by
the Mindanao current entering the Celebes Sea (Hoeksema,
2007). Researchers have long neglected the biota in the
southern islands of the archipelago due to continued
political unrest (e.g., Russ & Alcala, 1996; Carpenter &
Springer, 2005; Bos, 2011). In recent years however, new
records of shes have been observed in the Davao Gulf
(Bos & Gumanao, 2013; Bos & Smits, 2013) and a new
sh species Polydactylus longipes (Motomura et al., 2001)
was described. Furthermore, unique ecological discoveries,
such as a previously unknown corallimorph predator of the
crown-of-thorns sea star Acanthaster planci (Bos et al., 2008;
2011b) and a commensal relationship between shes and the
mushroom coral Heliofungia actiniformis (Bos, 2012)—so

757
RAFFLES BULLETIN OF ZOOLOGY 2014
far unique to the Davao Gulf—were reported. The present
description of U. nigromarginatus, new species, further
emphasises the biological and ecological distinctiveness of
the Davao Gulf.
Comparative material. Mulloidichthys flavolineatus
(Lacepède, 1801): ZMA.PISC.101.529, 3 ex., 154–200 mm
SL; Indonesia, West Sumatra, Pulu Babi, coll. E. Jacobsen,
April 1913; ZMA.PISC.132.456, 1 ex., 214 mm SL;
Indonesia, East Nusa Tenggara, coll. G.A.J. van de Sande,
6 December 1908; ZMA.PISC.101.528, 1 ex., 222 mm SL;
Indonesia, Siboga Expedition, 1899–1900.
Mulloidichthys martinicus (Cuvier, 1829): ZMA.
PISC.119.332, 2 ex., 159–168 mm SL; Dutch Antilles,
Curaçao, Caracas Bay, coll. C.J. van der Horst, 24 April 1920;
ZMA.PISC.108.086, 3 ex., 153–186 mm SL; Dutch Antilles,
Curaçao, Piscadera Bay, coll. H. Nijssen, 28 December 1966.
Mulloidichthys vanicolensis (Valenciennes, 1831): RMNH.
PISC.25449, 2 ex., 151–202 mm SL; East Indian Archipelago,
Sabang Bay, Pulu Weh, coll. P. Buitendijk, 1924; RMNH.
PISC.11245, 1 ex., 186 mm SL; Samoa, Savaii, coll. M.
Godeffroy, no date; ZMA.PISC.132.461, 1 ex., 213 mm SL;
Indonesia, Sumatra, coll. E. Jacobsen, no date.
Mullus auratus Jordan & Gilbert, 1882: RMNH.PISC.23345,
2 ex., 175–179 mm SL; Margarita Island, coll. S. Zaneveld,
6 February 1955.
Mullus surmuletus Linneaus, 1758: RMNH.PISC.26809,
2 ex., 162–182 mm SL; North Sea, Lightship Haaks,
1 July 1932; RMNH.PISC.35909, 1 ex., 172 mm SL;
The Netherlands, Oosterschelde, coll. V. Bakker, August
1983; ZMA.PISC.132.466, 2 ex., 213–256 mm SL; The
Netherlands, Den Helder, 21 May 1946.
Parapeneus barberinus (Lacepède, 1801): ZMA.
PISC.101.491, 2 ex., 139–151 mm SL; Indonesia, Makassar,
coll. M. Weber, 1888; ZMA.PISC.101.485, 1 ex., 153 mm SL;
Indonesia, South Sulawesi, Siboga Expedition, 1899–1900;
ZMA.PISC.101.494, 1 ex., 206 mm SL; Indonesia, coll. P.
Bleeker, 1842–1860; ZMA.PISC.101.497, 1 ex., 165 mm SL;
Indonesia, South Sulawesi, Siboga Expedition, 1899–1900.
Parapeneus heptacanthus (Lacepède, 1802): RMNH.
PISC.5737, 3 ex., 163–197 mm SL, East Indies, coll.
P. Bleeker, 1879; RMNH.PISC.467, 1 ex., 166 mm SL;
Indonesia, Macassar, coll. Piller, 1848; ZMA.PISC.101.422,
1 ex., 172 mm SL; Indonesia, Sulawesi, Ujung Pandang,
coll. M. Weber, 1888.
Parapeneus indicus (Shaw, 1803): RMNH.PISC.13333, 2 ex.,
177–195 mm SL; Indonesia, Java Sea, coll. P. Buitendijk,
1904–1907; ZMA.PISC.101.493, 2 ex., 159–192 mm SL;
Indonesia, coll. P. Bleeker, 1842–1860; ZMA.PISC.101.489,
1 ex., 181 mm SL; Indonesia, Sulawesi, Ujung Pandang,
coll. M. Weber, 1889.
Pseudupeneus maculatus (Bloch, 1793): ZMA.PISC.108.087,
2 ex., 164–164 mm SL; Dutch Antilles, Curaçao, Piscadera
Bay, coll. H. Nijssen, 28 July 1966; ZMA.PISC.136.256,
2 ex., 147–165 mm SL; Dutch Antilles, Curaçao, Caracas
Bay, coll. van der Horst, 1920; ZMA.PISC.136.257, 1 ex.,
219 mm SL; Caribbean, coll. Weger & Broeke, no date.
Pseudupeneus prayensis (Cuvier, 1829): ZMA.PISC.136.262,
3 ex., 171–180 mm SL; Senegal, coll. Vermeulen, 1906;
RMNH.PISC.486, 2 ex., 139–152 mm SL; Ghana, Ashanti,
coll. Pel, 1840–1855.
Upeneus tragula Richardson, 1846: RMNH.PISC.480, 2 ex.,
142–156 mm SL; Indonesia, Java, coll. Kuhl & van Hasselt,
1820; RMNH.PISC.13371, 2 ex., 131–135 mm SL; Indonesia,
Java Sea, coll. P. Buitendijk, 1906–1929; RMNH.PISC.459,
1 ex., 191 mm SL; Indonesia, Makassar, coll. Piller, no date.
Upeneus vittatus (Forskåll, 1775): RMNH.PISC.11479, 1 ex.,
205 mm SL; Samoa, coll. Godeffroy, June 1887; RMNH.
PISC.13355, 1 ex., 173 mm SL; Indonesia, Halmaheira,
coll. H.A. Bernstein, 1860–1865; ZMA.PISC.136.291, 2
ex., 176–192 mm SL; Indonesia, East Java, coll. Kromanly,
no date; ZMA.PISC.136.302, 1 ex., 237 mm SL; Indonesia,
Maluku, Buru Island, coll. Buitenzorg, 23 July 1913.
ACKNOWLEDGEMENTS
The support and contributions of J. Bayogan, G. Gumanao,
M. Saceda-Cardoza (Davao del Norte State College,
Philippines), N. Gallarda, C. Namoc, N. Namoc, and S.A.
Nitza are gratefully acknowledged. B. Hoeksema and R.
de Ruiter (Naturalis Biodiversity Center [NBC]) facilitated
my visits to Naturalis. A. Ouf (The American University in
Cairo [AUC], Egypt) supported the DNA analyses. J. Randall
(Bernice Pauahi Bishop Museum, Hawaii), A. Moustafa
(AUC), B. Reijnen (NBC), Z. Jaafar (National University of
Singapore), S. Nitza and an anonymous reviewer provided
valuable feedback on earlier versions of the manuscript. The
project was partially supported by a grant from the American
University in Cairo. The performed experiments complied
with the current laws of the Republic of the Philippines.
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