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Marine Biodiversity

, Volume 47, Issue 4, pp 1273–1285 | Cite as

Morphological and molecular divergence between Crenidens crenidens (Forsskål, 1775) and C. indicus Day, 1873 (Perciformes: Sparidae) and notes on a Red Sea endemic lineage of C. crenidens

  • Sergey V. Bogorodsky
  • Yukio Iwatsuki
  • Shabir A. Amir
  • Ahmad O. Mal
  • Tilman J. Alpermann
Red Sea Biodiversity

Abstract

Additional data, resulting from examination of newly collected material from the Red Sea, east coast of Africa, Arabian Gulf, Pakistan, and western coast of India, and a phylogenetic analysis of the COI barcoding region, confirms Crenidens crenidens (Forsskål) and C. indicus Day as valid species. The latter species was earlier regarded as a subspecies of C. crenidens. In addition, the analyses herein show that specimens from the Red Sea form a distinct monophyletic sub-clade within C. crenidens, characterized by low genetic divergence from specimens from the southwestern Indian Ocean. Close comparison of 34 morphological characters showed that specimens from South Africa and Mozambique differ from Red Sea specimens only in having slightly longer pelvic fins [4.6–4.9 in standard length (SL) vs. 4.8–6.1 in SL]. Examination of additional specimens of both species provided more assessment of inter- and intraspecific variation in meristic and morphometric characters. A new set of characters that help to distinguish C. indicus from C. crenidens is proposed: the former species has a deeper body and caudal peduncle; more scales between fifth dorsal-fin spine and lateral line; scales on top of head extending forward to vertical through posterior margin of pupil; longer pelvic fins; lips with tiny cirri; caudal fin blackish distally; and usually with obvious black spot at pectoral-fin axil. Crenidens indicus was previously reported from central Oman, Arabian Gulf, to Pakistan; herein its presence from the western coast of India, Gujarat and Mumbai (= Bombay), is confirmed. Descriptions of C. crenidens and C. indicus based on material examined, photographs of alive and fresh fishes and an updated key to the three known species of Crenidens are provided.

Keywords

Sparidae Crenidens Seabreams DNA barcoding Phylogenetic analysis Geographical distribution 

Introduction

Crenidens Valenciennes in Cuvier & Valenciennes, 1830 is a small group of commercially important omnivorous sparid fishes distributed in the coastal waters of the western and northern Indian Ocean. The genus formerly was monotypic with two recognized subspecies, C. crenidens crenidens (Forsskål, 1775) and C. crenidens indicus Day, 1873 (see e.g. Bauchot and Smith 1984; Randall 1995), until Iwatsuki and Maclaine (2013) redescribed Crenidens macracanthus Günther, 1874 from waters of the east coast of India and raised C. crenidens and C. indicus to species level. The genus is characterized in having dorsal-fin rays XI–XII,10–11; anal-fin rays usually III,10; dorsal profile of head slightly convex with a broad-based, slight convexity just in front of upper edge of eye; small horizontal mouth, maxilla reaching to below nostrils; dentition with an outer series of two (rarely three) rows of incisiform teeth in both jaws, the curved distal edge of each tooth with five denticulations (points), and 1–3 inner rows of molariform teeth behind incisors; scales on interorbital space extend anteriorly almost to a point vertically above the center of the eye; and naked preopercular flange.

Despite the fact that species of Crenidens are commercially important in parts of their distribution range (e.g. Middle East and Pakistan, see Bauchot and Smith 1984), few specimens have been studied in detail (see e.g. Iwatsuki and Maclaine 2013) and little is known about intraspecific variation in key morphological characters. Especially in C. crenidens, which is distributed from the Red Sea (its type locality in Jeddah, Saudi Arabia) along the east coast of Africa south to South Africa, some degree of intraspecific variation in morphological characters might correlate with persistence of geographically separated populations. Because of its geographical separation from the Indian Ocean and its unique evolutionary history with repeated cycles of (semi-)isolation due to Pleistocene sea level changes, the Red Sea is long known to harbor endemic populations of many fish species at various degrees of differentiation (see e.g. Klausewitz 1989 for a thorough review on the evolutionary history of the Red Sea and its consequences for the Red Sea ichthyofauna). In some taxa, such variation between Red Sea and Indian Ocean populations is of a subtle nature and as a consequence, it has only been detected by rigorous examination of a wide range of characters in a large sample of specimens. One recent example are the sibling labrid species Cheilinus quinquecinctus (Red Sea) and C. fasciatus (Indian Ocean) that long time have been considered one widespread species (see Bogorodsky et al. 2016). In such cases, the joint assessment of morphological variation together with evolutionary genetic divergence in an integrative taxonomical frame work can provide more profound evidence for species hypothesis than would be obtained by standard morphological analysis alone (see e.g., Dayrat 2005; Will et al. 2005). Because of the extension of the geographical distribution range of C. crenidens covering several marine subprovinces (i.e. Red Sea, Western Indian Ocean, Arabian Sea) and thereby spanning several biogeographic barriers (e.g. the Bab-al-Mandab – the transition between the Red Sea and the Gulf of Aden) some degree of regional partitioning of intraspecific genetic and/or morphological variation might be postulated.

During biodiversity surveys in Saudi Arabia, jointly conducted by the King Abdulaziz University and the Senckenberg Research Institute and Natural History Museum, specimens of C. crenidens were collected in shallow turbid waters in the Al Wajh bank, northern part of the Red Sea. We here perform a phylogenetic analysis with inclusion of sequences from voucher specimens of C. crenidens from the Red Sea and South Africa and from specimens of C. indicus from Pakistan and western India in order to assess potential intra- and interspecific molecular diversity. In addition, a direct and detailed comparison of morphological characters of specimens from these areas is carried out in order to reveal if populations from the outer parts of the distribution range of C. crenidens show any signs of morphological divergence. Because most publications (e.g. Smith and Smith 1986) include species accounts based on a mix of two species of Crenidens (considered earlier as subspecies C. crenidens crenidens and C. c. indicus), and moreover because one of the morphological characters (i.e. count of gill rakers) has been shown by Iwatsuki and Maclaine (2013) to greatly overlap, a new combination of characters to distinguish the two species is provided.

Herein, descriptions of specimens of Crenidens crenidens from the Red Sea and south-east coast of Africa and of C. indicus from Kuwait, Pakistan and western India are detailed together with respective diagnosis. In addition, pictures showing the typical coloration of fresh and alive fishes are included, as well as an updated key to the three known species of Crenidens.

Material and methods

Institutional abbreviations based mostly on Eschmeyer et al. (2017). Specimens from the following institutions were examined: King Abdulaziz University Marine Museum, Jeddah (KAUMM); South African Institute for Aquatic Biodiversity, National Research Foundation, Grahamstown (SAIAB); Senckenberg Research Institute and Natural History Museum, Frankfurt (SMF); Smithsonian Institution National Museum of Natural History, Suitland MD (USNM). Number in square brackets after collection number is tissue voucher number.

Meristic and morphometric methods followed Hubbs and Lagler (1964), Iwatsuki et al. (2007), and Iwatsuki and Heemstra (2010, 2011). The length of specimens is presented as standard length (SL) measured from anteriormost point of upper lip to the base of caudal fin (end of hypural plate). Count of pored scales in lateral line includes count from anteriormost tubed scale above opercular margin to the end of hypural plate, in case if scale partly overlaps end of hypural plate, such scale was included in count of lateral line scales; additional pored scales on caudal-fin base counted separately. Proportional measurements rounded to the nearest 0.1 mm for specimens less than 80 mm SL, and to 0.5 mm for specimens larger than 80 mm SL. Morphometric data presented are given as ratio to standard length in the text and percentages of standard length in Table 1 for easier comparison with published data; data given in the Table 1 and the description is based on material examined in this study, data given in diagnosis and key to the species is a combination of data from Iwatsuki and Maclaine (2013) and the present study; frequency of count of pored lateral line scales and developed gill rakers on first gill arch is included in the Table 2.
Table 1

Morphometric and meristic data for Crenidens crenidens and C. indicus. Standard length is expressed in millimeters, all other measurements are expressed as percentage of standard length. Three diagnostic characters (body depth, caudal peduncle depth, and pelvic-fin length) are marked in bold

Specimen

Crenidens crenidens Red Sea

mean

Crenidens crenidens South Africa & Mozambique

mean

Crenidens indicus

mean

Crenidens indicus, SMF 21479, Mumbai

Standard length, mm

108.5–188.0

n = 15

114.9–188.0

n = 8

160.0–220.0

n = 12

108.0

Body depth (at V origin)

38.6–43.1

41.0

40.5–45.1

42.4

45.6–51.2

47.5

45.4

Body depth (measured at A origin)

31.3–36.3

33.3

32.5–36.8

34.2

36.8–39.1

37.7

37.3

Head length

25.7–29.7

27.5

26.4–28.9

27.6

28.8–32.4

30.7

28.2

Body width

14.9–19.1

17.6

14.8–18.0

15.9

15.6–20.0

17.4

15.3

Snout length

10.4–12.6

11.2

10.0–11.6

11.0

9.4–11.1

10.5

9.9

Orbit diameter

8.0–9.8

8.9

9.0–11.6

10.1

8.2–10.6

9.4

9.0

Dermal eye opening

6.6–8.1

7.5

7.7–10.2

8.4

7.5–10.0

8.6

7.7

Interorbital width, bony

8.1–9.1

8.5

7.9–8.3

8.1

10.0–11.7

10.8

9.1

Interorbital width, with membrane

9.5–10.9

10.0

9.5–11.6

10.4

10.8–12.8

11.7

Upper-jaw length

6.4–7.7

7.1

6.4–9.3

7.3

7.2–10.5

8.9

8.1

Caudal-peduncle depth

10.2–11.6

10.9

10.7–11.7

11.3

12.6–13.2

12.9

13.2

Caudal-peduncle length

15.9–19.1

17.3

16.2–18.8

17.2

16.4–19.3

18.0

16.2

Predorsal length

37.9–42.2

40.0

38.4–41.7

40.6

43.1–47.8

45.2

42.8

Preanal-fin length

61.4–72.7

67.9

63.8–68.6

67.0

69.4–75.3

71.6

69.1

Prepelvic length

34.3–40.7

36.6

33.4–37.4

35.8

36.8–41.3

39.2

36.7

Base of dorsal fin

53.0–57.2

55.6

54.1–58.6

56.5

54.2–58.6

56.4

57.4

Base of anal fin

13.9–17.8

16.5

16.6–18.8

17.9

17.3–19.4

18.3

18.3

Caudal-fin length

22.1–27.0

25.4

26.6–28.3

27.4

29.6–31.7

30.3

27.8

Pelvic-spine length

13.5–16.0

14.6

13.4–16.1

14.7

16.2–16.9

16.5

14.4

Pelvic-fin length

16.4–20.9

19.1

20.4–21.9

21.3

22.5–27.2

26.0

23.6

Pectoral-fin length

32.7–37.9

34.6

35.4–37.8

36.5

37.4–43.3

40.5

33.8

First dorsal-fin spine

5.0–6.6

5.8

5.3–6.6

5.9

5.6–8.4

6.8

6.5

Second dorsal-fin spine

9.0–10.8

10.3

10.0–13.3

11.4

8.8–12.9

11.1

10.7

Third dorsal-fin spine

13.2–15.6

14.1

13.1–16.4

15.0

12.5–17.3

14.8

15.1

Fourth dorsal-fin spine

12.8–15.8

14.7

13.3–16.3

15.1

14.4–18.8

16.6

16.2

Fifth dorsal-fin spine

11.6–16.0

13.4

11.9–15.8

14.2

13.8–18.3

16.1

15.6

Last dorsal-fin spine

8.5–10.9

9.7

9.1–12.4

10.4

9.0–12.1

11.0

13.4

Longest dorsal-fin ray

9.0–11.5

10.2

10.1–12.5

11.1

10.8–12.9

11.6

14.4

First anal-fin spine

3.1–5.5

4.6

3.8–5.6

4.9

4.8–6.1

5.3

4.2

Second anal-fin spine

11.2–13.5

12.3

11.2–12.6

11.9

12.5–13.9

13.1

13.2

Third anal-fin spine

10.6–12.4

11.5

10.6–12.7

11.7

11.4–13.6

12.6

13.0

First anal-fin ray

10.3–12.8

11.8

10.7–13.8

12.4

11.8–15.3

12.6

13.4

suborbital depth

5.1–6.5

5.9

4.8–6.0

5.4

5.0–6.4

5.7

5.6

Posteriormost jaw

7.5–10.0

8.8

7.1–8.8

8.2

7.2–10.6

9.3

8.4

Meristics

 Dorsal-fin rays

XI,10–11

XI,11

XI,10–11

XI,11

XI,10–11 (rarely XII,10)

XI,10–11

XI,11

 Anal-fin rays

III,8–10

III,10

III,10

III,10

III,9–10

III,10

III,10

 Pectoral-fin rays

14–16

14–15

13–14

14

13–14

14

14

 Tubed scales

52–57

Table 1

52–57

Table 1

50–57

Table 1

55/54

 Scales above LL

5.5–6.5

6.5

6.5–7.5

6.5

5.5–6

6

6.5

 Scales below LL

11.5–14.5

12.5

11.5–13.5

12.5

12.5–13.5

13

13.5

 Scales between fifth dorsal-fin spine and lateral line

5.0–5.5

5.5

5.0–5.5

5.5

6

6

6.5

 Scales between tenth dorsal-fin spine and lateral line

4.5–5.5

4.5 or 5.5

4.5–5.5

4.5 or 5.5

6

6

6

 Rows of scales on cheek

3–5

3 or 4

3–4

3 or 4

4–5

4

4

 Rows of scales on opercle

5–6

5

4–5

4 or 5

4–5

4

4

 Developed gill rakers

4–7 + 9–11 = 14–18

Table 1

5–7 + 9–11 = 14–18

Table 1

5–7 + 9–11 = 14–17

Table 1

6 + 10 = 16

 Gill rakers incl. rudim.

5–10 + 9–11 = 15–20

 

8–10 + 9–12 = 17–21

 

6–8 + 10–12 = 15–20

 

7 + 11 = 18

Table 2

Frequency distribution of pored lateral-line scales and developed gill rakers on lower limb of first gill arch for Crenidens crenidens and C. indicus

Tubed lateral-line scales

50

51

52

53

54

55

56

57

mean

Crenidens crenidens Red Sea

-

-

6

7

7

4

3

1

54

Crenidens crenidens South Africa

-

-

1

3

6

1

1

1

54

Crenidens indicus

2

3

4

1

2

1

1

2

53

Developed lower gill rakers

9

10

11

mean

Crenidens crenidens Red Sea

6

6

3

10

Crenidens crenidens South Africa

4

6

1

10

Crenidens indicus

2

6

1

10

A maximum likelihood phylogenetic analysis of the barcoding portion of the mitochondrial COI gene of specimens of Crenidens crenidens and C. indicus by maximum likelihood (ML) was performed (Folmer et al. 1994; Hebert et al. 2004), in order to assess the evolutionary divergence of the two species and intraspecific genetic variation. Genomic DNA was isolated either with a DNeasy tissue kit (Qiagen, Hilden, Germany) or according to the protocol developed by the Canadian Centre for DNA Barcoding (Ivanova et al. 2006) from tissue samples. Amplification of a 652 bp sequence of the mtCOI gene was carried out with the universal, M13-tailed primer set COI-3 from Ivanova et al. (2007; partly taken from Ward et al. 2005) according to the PCR protocol in this study or the modified protocol from Geiger et al. (2014). Amplicons were Sanger sequenced from both ends with primers M13F (−21) and M13R (−27) (Messing 1983) and contigs were assembled in Geneious Pro 5.4.4 (Biomatters, Auckland, New Zealand). An alignment of COI sequences obtained in this study, and sequences of C. crenidens available from GenBank was constructed with the same software. A unrooted maximum likelihood (ML) phylogenetic tree was then inferred inferred in PhyML 3.0 (Guindon et al. 2010; Guindon and Gascuel 2003) under the TVM + Γ model, the best fitting model of nucleotide substitution as estimated according to AIC scores in jModelTest (Posada 2008, Guindon and Gascuel 2003). Reliability of branch support was assessed by 200 bootstrap replicates. From the same sequence alignment, uncorrected pairwise distances and pairwise K2P-distances were estimated for all aligned sequences in PAUP* (Swofford 1998) and intra- and interlineage divergence of C. crenidens and C. indicus and of specimens of C. crenidens from the Red Sea and from the western Indian Ocean were estimated in the computer program Species Delimitation (Masters et al. 2011). All computational analyses were conducted via respective software plugins in Genious Pro. Material for the genetic analysis is listed in Appendix 1.

Results

Family Sparidae Rafinesque, 1818.

Genus Crenidens Valenciennes in Cuvier & Valenciennes, 1830.

Revised key to the species of Crenidens

1a. Dorsal-fin rays XII,10; second anal-fin spine much longer (1.3–1.4 times) than third; incisor-like teeth with five, subequal in size, points ……………………………….C. macracanthus.

1b. Dorsal-fin rays XI,10–11; second anal-fin spine subequal to or only slightly (0.9–1.3 times) longer than third; incisor-like teeth with five points, three median points much larger than outer point on each side ……………………………….2.

2a. Body moderately deep, the depth 2.2–2.9 in SL; scale rows between fifth dorsal-fin spine base and lateral line 5–5.5; scales on top of head extending forward to vertical through posterior margin of eye; caudal peduncle depth 8.5–9.8 in SL, 1.5–1.6 in its length; pelvic-fin length 4.6–6.1 in SL; lips smooth; small faint blackish spot dorsally in pectoral-fin axil; caudal fin usually uniform pale gray ……………………………….C. crenidens.

2b. Body deep, the depth 2.0–2.3 in SL; scale rows between fifth dorsal-fin spine base and lateral line 6–6.5; scales on top of head extending forward to vertical through posterior margin of pupil; caudal peduncle depth 7.7–8.2 in SL, 1.4 in its length; pelvic-fin length 3.9–4.3 in SL; lips with tiny prickle-like cirri; usually obvious blackish spot dorsally in pectoral-fin axil; caudal fin blackish distally ……………………………….C. indicus.

Crenidens crenidens (Forsskål, 1775)

Karanteen Seabream

Sparus crenidens Forsskål, 1775: iv (type locality: Red Sea, Saudi Arabia, Jeddah; lectotype: ZMUC P50551).

Crenidens forskalii Valenciennes in Cuvier & Valenciennes, 1830: 378 (type locality: Red Sea, Egypt, Suez and Eritrea, Massawa) — Rüppell 1852: 7 (Red Sea); Klunzinger 1870: 748 (El Quseir); Klunzinger 1884: 45 (Red Sea); Tillier 1902: 296 (Port Said); Pellegrin 1907: 203 (Madagascar); Chabanaud 1932: 829 (Bitter Lake, Suez Canal); Iwatsuki and Maclaine 2013: 245 (Red Sea, designated as the lectotype, MNHN 8744, largest specimen, 122 mm SL).

Crenidens crenidens crenidens — Marshall 1952: 234 (Sanafir Isl.); Golani and Bogorodsky 2010: 34 (Red Sea).

Crenidens crenidens — Norman 1929: 380 (Gulf of Suez); Chabanaud 1934: 159 (Lake Timsah); Tortonese 1935: 182 (Red Sea); Gruvel 1936: 169 (Suez Canal); Smith 1949: 275 (South Africa); Budker and Fourmanoir 1954: 324 (Hurghada); Fourmanoir 1957: 135 (Madagascar); Bauchot and Smith 1984: SPARID (western Indian Ocean); Tortonese 1983: 107 (Jeddah); Dor 1984: 159 (Red Sea); Smith and Smith 1986: 585 (western Indian Ocean); Goren and Dor 1994: 43 (Red Sea); Sommer et al. 1996: 247 (Somalia); Heemstra and Heemstra 2004: 222 (South Africa); Iwatsuki and Maclaine 2013: 244, Fig. 1c (Red Sea, East Africa, along the east coast of Africa to Aliwal Shoal, South Africa).
Fig. 1

Crenidens crenidens. (a) SMF 35159 [KAU13-118], 121.0 mm SL, fresh, Al Wajh bank, Saudi Arabia, Red Sea; (b) SMF 35850 [KAU13-420], 187.0 mm SL, fresh, Al Wajh bank, Saudi Arabia, Red Sea; (c) alive, Sharm el Naga, Safaga, Red Sea. Photos by S.V. Bogorodsky (a & b), A. Ryanskiy (c)

Materials examined (additional to that examined by Iwatsuki and Maclaine (2013)):

Crenidens crenidens. RED SEA, Israel: SAIAB 42685, 7: 121.0–188 mm, Eilat. Saudi Arabia: KAUMM 164 [KAU13-120], 10: 65.0–122.0 mm, 60 km south of Al Wajh, 11 June 2013; KAUMM 425 [KAU13-405], 1: 138.5 mm, 60 km south of Al Wajh, 15 June 2013; KAUMM 426 [KAU13-404], 1: 143.5 mm, 60 km south of Al Wajh, 15 June 2013; KAUMM 427 [KAU13-407], 1: 147.0 mm, 60 km south of Al Wajh, 15 June 2013; KAUMM 249, 1: 86.0 mm, 60 km south of Al Wajh, 16 June 2013; SMF 35159 [KAU13-118 & 119], 11: 61.2–121.0 mm, 60 km south of Al Wajh, 11 June 2013; SMF 35848 [KAU13-406], 1: 132.5 mm, 60 km south of Al Wajh, 15 June 2013; SMF 35849 [KAU13-408], 1: 140.5 mm, 60 km south of Al Wajh, 15 June 2013; SMF 35850 [KAU13-420], 1: 187.0 mm, 60 km south of Al Wajh, 15 June 2013; SMF 35301, 2: 85.0–91.0 mm, 60 km south of Al Wajh, 16 June 2013. Yemen: USNM 49290, 2: 112.0 mm, Gulf of Aden. Tanzania: SAIAB 10435, 1: 80.5 mm. Mozambique: SAIAB 1376, 1: 102.0 mm, Maputo; SAIAB 10433, 2: 99.5–113.5 mm, Inhaca Island; SAIAB 10460, 1: 58.0 mm, Ponta Maona; SAIAB 10464, 3: 28.0–188.0 mm, Delagoa Bay. South Africa: SAIAB 8049, 1: 106.0 mm, Eastern Cape; SAIAB 10454, 1: 77.0 mm, KwaZulu Natal; SAIAB 10458, 1: 159.5 mm, KwaZulu Natal; SAIAB 10459, 1: 99.5 mm, KwaZulu Natal; SAIAB 16154, 1: 111.0 mm, KwaZulu Natal; SAIAB 16566, 1: 118.0 mm, KwaZulu Natal; SAIAB 38063, 1: 155.5 mm, KwaZulu Natal; SAIAB 88324, 5: 75.5–115.0 mm, KwaZulu Natal; SAIAB 193756, 1: 70.5 mm, KwaZulu Natal.

Diagnosis

A species of Crenidens with the following combination of characters: dorsal-fin rays XI,10–11, usually XI,11; anal-fin rays III,8–10, usually III,10; pectoral-fin rays 13–16, rarely 13 or 16; pored lateral-line scales 52–57 (usually 52–54); scale rows between fifth dorsal-fin spine and lateral line 5–5.5; scales on top of head extending forward to vertical through posterior margin of eye; body moderately deep, the depth 2.2–2.9 in SL; caudal peduncle moderately low, the depth 8.5–9.8 in SL and 1.5–1.6 in its length; lips smooth; incisor-like teeth with five points, outer point on each side of tooth smaller than three median points; second and third anal-fin spines nearly equal in length, the length of third spine 0.9–1.2 in the second; pelvic fins moderately short, 4.6–6.1 in SL; caudal fin uniform pale gray.

Description

Counts and proportional measurements of Crenidens crenidens are given in Tables 1 and 2 separately for Red Sea specimens and specimens from Tanzania, Mozambique, and South Africa.

Body somewhat oval, compressed, and moderately deep, the maximum depth 2.2–2.6 in SL. Dorsal profile of head slightly convex with a broad-based, slight convexity just in front of upper edge of eye; ventral profile nearly straight. Anterior nostril oval, posterior nostril larger, narrowly oval with flap. Orbit diameter subequal to interorbital width. Mouth horizontal and small, the maxilla reaching to below nostrils or to below anterior margin of eye, hind margin of maxilla concealed by infraorbitals or sometimes exposed. Lips smooth. Jaws usually with two series of incisor-like teeth (third series present mainly in upper jaw but very weak), teeth of outer series larger; incisor-like teeth with five points, outer point on each side of tooth smaller than three median points, tending to form a flat cutting edge at each incisor-like tooth; outer teeth movable; 1–3 inner rows of small molariform teeth behind of incisor-like teeth at posterior part of jaws. Posterior margin of preopercle generally rounded and weakly serrated. Predorsal length subequal to body depth, and clearly less than dorsal-fin base length. Caudal peduncle moderately low, the depth 8.5–9.8 in SL and 1.5–1.6 in its length. Pectoral-fin base rounded posteriorly, the fin tip reaching slightly beyond vertical at anus, but not reaching anal-fin origin, its length clearly greater than head length. Pelvic fins longer than longest dorsal-fin spine, fin tip clearly not reaching beyond vertical at anus, the length 4.6–4.9 in SL in Red Sea specimens and 4.8–6.1 in SL in specimens from east coast of Africa. First to fourth dorsal-fin spines progressively longer, fourth dorsal-fin spine usually longest and much greater than snout length. Anal-fin origin below fourth dorsal-fin ray, second and third spines strong, nearly equal in length, the length of third spine 1.1 in second. Caudal fin weakly forked, each lobe with rounded posterior margin and somewhat pointed tip.

Scales ctenoid, anus mostly enclosed by scales or with a small naked area before anus; suborbital and area behind eye naked, lower cheek with 3–4 (rarely five) rows of scales, opercle with 4–5 (rarely six) rows of scales; preopercle flange naked; lateral line gently curved, subparallel to curved dorsal profile from nape to caudal peduncle, with 52–57 (usually with 52–54) pored scales, pored scales continue into dorsal-fin base; scale rows between fifth dorsal-fin spine and lateral line 5–5.5, usually 5.5; scale rows between tenth dorsal-fin spine and lateral line 4.5–5.5; pectoral-fin base scaly; interorbital space scaleless, scales on top of head extending forward to vertical through posterior margin of eye; maxilla naked; no scaly sheath on spinous portion of dorsal and anal fins; soft dorsal and anal fins with no scales but with weak scaly sheaths anteriorly and moderate posteriorly. Gill rakers lanceolate, with denticles on hind margin and short filament at tip; developed gill rakers 4–7 + 9–11 = 14–18, gill rakers including rudiments 5–10 + 9–12 = 15–21.

Coloration (Fig. 1). Silvery with poorly defined dusky spot in scale center, resulting in a striped effect below lateral line, more obvious in alive individuals; a very small faint blackish spot dorsally in axil of pectoral fin; dorsal and anal fins with gray spines and rays and semitranslucent membranes, caudal fin uniform pale gray, rarely little dusky distally; margin of spinous portion of dorsal fin narrowly black; denticulations of incisiform teeth brown; iris white, sometimes with small dark brown mark dorsally.

Size. Attains about 30 cm of total length (Smith and Smith 1986).

Distribution and habitat

Crenidens crenidens known from the Red Sea and Gulf of Aden south to Madagascar and South Africa (East London). It was one of the first Lessepsian migrants into the Suez Canal and eastern Mediterranean Sea, its occurrence in the Great Bitter Lake (Suez Canal) is documented by the specimen SMNS 3309, collected in 1887; at present reported from Libya, northern Egypt, Israel, and Turkey (Bilecenoglu et al. 2002; Golani et al. 2002). Zajonz et al. (2000) reported C. indicus from Socotra based on material collected by Steindachner (1902). Several specimens, recently collected in estuarine areas of Socotra, were identified as C. crenidens (Zajonz et al., in prep.). According published data and a search of museum collections, the species is still unknown from Kenya.

Inhabits coastal shallow – often turbid – waters in estuaries and bays, reported to 15 m depth; specimens collected during the study were collected from depth less than 2 m; usually in small groups; feeds on benthic algae, including a variety of small invertebrates associated with algal turf.

Remarks

Fricke (2008) listed the specimen collected from Jeddah (ZMUC P50551) as a syntype of Crenidens crenidens; later Iwatsuki and Maclaine (2013) designated it as a lectotype and recognized three species in the genus: C. crenidens, C. indicus, and C. macracanthus. The latter is a very rare species, known from the east coast of India only and can easily be distinguished from the other two species in having XII dorsal-fin spines (vs. XI spines), a second anal-fin spine much longer than the third spine, with a ratio of 1.3–1.4 (vs. spines subequal or second little longer, and a ratio of 0.9–1.2), fewer pored lateral-line scales 47–48 (vs. 50–57), and incisor-like teeth with five points of subequal size (vs. three median points much larger than outer point on each side).

After comparison between C. crenidens and C. indicus, Iwatsuki and Maclaine (2013) found that C. crenidens can easily be differentiated from C. indicus by its 4.5 scale rows between the tenth dorsal-spine base and lateral line (vs. 5.5 or 6.5), gill rakers in the lower arch (9 or 10 in C. crenidens vs. 10–12 in C. indicus), a dark spot dorsally in the pectoral-fin axil (absent in C. crenidens vs. present in C. indicus) and a slender body (2.4–2.9 in SL for C. crenidens vs. a relatively deeper body 2.1–2.3 in SL for C. indicus). However, they gave a count of gill rakers on the lower limb of 10–11 in their Table 1 instead of 9–10. Moreover, these authors omitted depth of caudal peduncle as a diagnostic character. Based on examination of more material, the combination of the following characters can help to distinguish C. crenidens from C. indicus and are provided in the updated key: body depth; depth of caudal peduncle; length of pelvic fins; scales count between fifth dorsal-fin spine and lateral line; extension of scales on top of head; presence or absence of tiny cirri on lips; presence or absence of black spot in pectoral-fin axil; and color of caudal fin. Some specimens of C. indicus may have an obscure black spot in the pectoral-fin axil. Count of gill rakers is not useful because of a great overlap in this character in the two species. Iwatsuki and Maclaine (2013) provided data on the basis of 15 specimens from the Red Sea only, but they gave the distribution range of the species in the western Indian Ocean south to South Africa. Herein, the examination of additional specimens of C. crenidens from a larger portion of its distribution range extends the known variation in the following meristic and morphometric characters: number of rays in dorsal, anal, and pectoral fins, count of pored lateral-line scales, and body depth. Comparison of specimens from the Red Sea and south-western Indian Ocean (Tanzania, Mozambique, and South Africa) demonstrates that there is no evidence of meristic differences, and only one morphometric character exhibits a difference between populations: pelvic fins are generally shorter in Red Sea specimens (4.6–4.9 in SL vs. 4.8–6.1 in SL).

Crenidens indicus Day, 1873

Indian Seabream

Crenidens indicus Day, 1873: clxxxvi (type locality: Pakistan, Karachi; lectotype: ZSI 1774).

Crenidens crenidens — Carpenter et al. 1997: 181 (Arabian Gulf).

Crenidens crenidens indicus — Randall 1995: 225 (Oman); Iwatsuki and Maclaine (2013): 34 (Gulf of Oman).

Crenidens indicus — Iwatsuki and Maclaine 2013: 244, Fig. 1b (India and Arabian Sea; designated the lectotype ZSI 1774, ca. 144 mm SL); Siddiqui et al. 2014: 82 (Pakistan); Psomadakis et al. 2015: 262 (Pakistan).

Materials examined (in additional to that examined by Iwatsuki and Maclaine (2013)):

Crenidens indicus. Kuwait: SMF 21501, 1: 59.2 mm. India: SMF 21479, 1: 108.0 mm, Mumbai. Pakistan: MUFS 36567, 1: 156.0 mm; MUFS 36568, 1: 149.5 mm; MUFS 36569, 1: 149.0 mm; MUFS 36570, 1: 204.0 mm; PMNH 52003, 1: 165.0 mm; PMNH 54617, 1: 183.0 mm; PMNH 54618, 1: 166.0 mm; PMNH 54619, 1: 160.0 mm; PMNH 54621, 1: 220.0 mm; PMNH 54622, 1: 171.0 mm; PMNH 54623, 1: 190.0 mm; PMNH 54624, 1: 180.0 mm; PMNH 54625, 1: 202.0 mm; PMNH 54626, 1: 179.0 mm.

Diagnosis

A species of Crenidens with the following combination of characters: dorsal-fin rays XI,11; anal-fin rays III,9–10, usually 10; pectoral-fin rays 13–16 (usually 14); pored lateral-line scales 50–57; scale rows between fifth dorsal-fin spine and lateral line 6–6.5; scales on top of head extending forward to vertical through posterior margin of pupil; body somewhat deep, the depth 2.0–2.3 in SL; caudal peduncle moderately deep, the depth 7.7–8.2 in SL, 1.4 in its length; lips, especially lower, covered with tiny prickle-like cirri; incisor-like teeth with five points, outer point on each side of tooth smaller than three median points; second anal-fin spine subequal or little longer than the third, the length of third spine 1.0–1.3 in the second; pelvic fins moderately long, 3.9–4.3 in SL; usually an obvious black spot at pectoral-fin axil; caudal fin blackish distally.

Description

Counts and proportional measurements of Crenidens indicus are given in Tables 1 and 2.

Body somewhat oval, compressed, and somewhat deep, the maximum depth 2.0–2.3 in SL. Dorsal profile of head slightly convex with a broad-based, slight convexity just in front of upper edge of eye; ventral profile nearly straight. Anterior nostril oval, posterior nostril larger, narrowly oval with flap. Orbit diameter subequal to interorbital width. Mouth horizontal and small, the maxilla reaching to below nostrils or to below anterior margin of eye, hind margin of maxilla concealed by infraorbitals or sometimes exposed. Lips covered with fine structures, tiny prickle-like cirri, more numerous in lower lip. Dentition as in C. crenidens. Posterior margin of preopercle generally rounded and weakly serrated. Predorsal length subequal to body depth. Caudal peduncle moderately deep, the depth 7.7–8.2 in SL, 1.4 in its length. Pectoral-fin base rounded posteriorly, the fin tip reaching slightly beyond vertical at anus or reaching anal-fin origin, its length clearly greater than head length. Pelvic fins longer than longest dorsal-fin spine, fin tip reaching anus, the length 3.9–4.3 in SL. First to fourth dorsal-fin spines progressively longer, fourth dorsal-fin spine usually longest and much greater than snout length. Anal-fin origin below fourth dorsal-fin ray, second and third spines strong, nearly equal in length, the length of third spine 1.0–1.3 in the second. Caudal fin weakly forked, each lobe with rounded posterior margin and somewhat pointed tip.

Scales ctenoid, anus mostly enclosed by scales; suborbital and area behind eye naked, lower cheek with 4–5 rows of scales, opercle with 4–5 (rarely 6) rows of scales; preopercle flange naked; lateral line gently curved, subparallel to curved dorsal profile from nape to caudal peduncle, with 50–57 pored scales, pored scales continue into dorsal-fin base; scale rows between fifth dorsal-fin spine and lateral line 6–6.5; scale rows between tenth dorsal-fin spine and lateral line 5.5–6.5; pectoral-fin base scaly; interorbital space mainly scaleless, scales on top of head extending forward to vertical through posterior margin of pupil; maxilla naked; no scaly sheath on spinous portion of dorsal and anal fins; soft dorsal and anal fins with no scales but with weak scaly sheaths anteriorly and moderate posteriorly. Gill rakers as in C. crenidens; developed gill rakers 4–7 + 9–11 = 14–18, gill rakers including rudiments 5–10 + 9–12 = 15–21.

Coloration (Fig. 2). Silvery with poorly defined dusky spot in scale center, resulting in a striped effect, more obvious ventrally; obvious large to a very small faint blackish spot dorsally in axil of pectoral fin; dorsal fin with pale gray spines and rays and gray membranes, anal fin with gray spines and dusky soft portion, caudal fin usually dusky basally shading to blackish distally; margin of spinous portion of dorsal fin narrowly black; denticulations of incisiform teeth brown; iris yellowish, sometimes with small dark brown mark dorsally.
Fig. 2

Crenidens indicus. (a) NF591, 185.0 mm SL, fresh, Gujarat, India; (b) PMNH 54623, 190.0 mm SL, fresh, Pakistan; (c) SMF 21479, 108.0 mm SL, preserved, Mumbai, India. Photos by G. Khedkar (a), S.A. Amir (b), S.V. Bogorodsky (c)

Distribution and habitat

Iwatsuki and Maclaine 2013, p. 247) reported that C. indicus occurs along the coast of India and Arabian Sea following Bauchot and Smith (1984). However, the record from India is questionable, and the conclusion is that it is either not distributed along the coast of India or it might be an extremely rare occurrence in that area. We did not find any evidence of the presence of C. indicus from the Red Sea. A single specimen from the western coast of India (Mumbai = Bombay) examined herein, as well as the specimen collected from Gujarat (G.D. Khedkar, pers. comm.) included in phylogenetic analyses, confirm occurrence of the species in Indian waters. Westernmost confirmed record from the central Oman (Randall 1995). Occurs in shallow, often turbid waters.

Remarks

Siddiqui et al. (2014) reviewed 14 sparid species in Pakistani waters including description of four specimens of C. indicus, but did not include a comparison with C. crenidens. As noted in remarks for C. crenidens, this species differs from C. indicus by a set of characters provided in detail in the key. Among these characters, three were found in addition to those used by Iwatsuki and Maclaine (2013) to be useful for identification of both species: examined specimens of C. indicus are characterized in extension of scales on top of head forward to vertical through posterior margin of pupil, whereas scales extending to vertical through posterior margin of eye in C. crenidens. Furthermore, specimens of C. indicus are characterized by relatively longer pelvic fins (3.9–4.3 in SL vs. 4.6–6.1 in SL in C. crenidens) and by possessing prickle-like cirri on the lips (more numerous on the lower lip), whereas lips are smooth in C. crenidens (Fig. 3).
Fig. 3

Lower lip of two species of Crenidens. (a) C. crenidens, SMF 35850; (b) C. indicus, SMF 21479. Arrow showes tiny prickle-like cirri. Photos by S. Tränkner

Phylogenetic analyses

The maximum likelihood (ML) analysis resulted in a clear separation of C. indicus and C. crenidens by placement of specimens of either species into reciprocally monophyletic clades with high bootstrap support (100%, see Fig. 4). Closest uncorrected interspecific distance was 6.8% (K2P distance: 7.3%), and the ratio between average intraspecific and interspecific distances was 0.05 (0.05) and 0.12 (0.12) for C. indicus and C. crenidens, respectively. In addition, reciprocally monophyletic placement of specimens of C. crenidens from the Red Sea (including one from the Mediterranean) and the Indian Ocean, respectively, was observed (see Fig. 4). The divergence between these evolutionary lineages was far less prominent with the closest uncorrected distance of 1.4% (K2P: 1.4%) corresponding to eight nucleotide substitutions in 652 bp that were found in all specimens of the respective lineages. Only one of these diagnostic mutations resulted in a change in the amino acid sequence in the Indian Ocean lineage (compared to C. indicus and C. crenidens from the Red Sea). This lineage also diverged much more in comparison to the Red Sea lineage as is evident from substantially longer branch length in the ML analysis (see Fig. 4). As divergence within the two geographically separated lineages of C. crenidens was relatively low, the ratio between intra- and interlineage divergence was still relatively high with 0.11 (K2P: 0.11) and (0.2) for specimens from the Red Sea and the Indian Ocean, respectively.
Fig. 4

Maximum likelihood phylogeny of COI barcoding sequences of specimens of Crenidens crenidens and C. indicus. Values on branches represent percent bootstrap support from 200 replicates. The scale bar represents average nucleotide substitutions. *Original branch length: 0.146

Discussion

Integrative taxonomic study, based on a combination of morphological examination (including comparison of coloration – especially among alive and fresh specimens) and of molecular phylogenetic analyses, can help in distinguishing among closely related species of fish (see e.g. Bogorodsky et al. 2016; Bañón et al. 2016). Here, we compiled morphological and molecular data for two species of CrenidensC. crenidens and C. indicus – that historically were considered subspecies, before they were formally raised to species level based on comparative morphology alone (Iwatsuki and Maclaine 2013). Moreover, the detailed analysis of morphological characters in both species provided herein, identified several additional distinctive features that can be helpful in their identification (see remarks for both species for details). Together with this growing evidence of morphological divergence, a high level of intraspecific molecular divergence was obvious from the maximum likelihood phylogenetic analysis of COI barcoding sequences (Fig. 4). Such high genetic divergence is indicative of evolutionary separation over time scales of millions of years rather than of recent divergence (see e.g., the compilation in Lessios (2008) for geminate species pairs across the Central American Isthmus with 1 to 2% K2P-distance divergence in COI per million years). However, as so far no samples from the third congener, C. macracanthus, are available for the assessment of intrageneric phylogenetic relationships, the relative degree of relatedness among the three species remains to be assessed.

Interestingly, the maximum likelihood analysis also identified two unique evolutionary lineages in C. crenidens that corresponded to sequences of either Red Sea (containing also one specimen from the Mediterranean Sea) or western Indian Ocean origin (all sequence were from South Africa except ODUT-B15.78 for which its origin, due to its recorded collection locality “Saif Market, Kuwait City”, is still uncertain). As the Mediterranean population of C. crenidens is the result of Lessepsian migration from the Red Sea we still refer to this lineage as Red Sea “endemic” in its evolutionary context (see e.g. Por 1978; Bariche et al. 2015). The relatively low divergence among the two lineages (K2P distance of 1.4%) still corresponds to an evolutionary divergence time of at least several hundred thousand years under the above mentioned evolutionary rate. However, the relatively high variation in evolutionary rates within species (and between sister species) is evident from the about threefold higher number of acquired nucleotide substitutions in the Indian Ocean lineage when compared to the lineage from the Red Sea. Nevertheless, the reciprocally monophyletic geographical lineages might have started to diverge as a consequence of cyclic Pleistocene climate variations with their accompanying sea level changes. These cycles of (near) complete isolation of the Red Sea and subsequent re-opening of its oceanographic connection to the Indian Ocean have been considered the most important factor in triggering the divergence of fish populations from these regions. In many cases, it has been hypothesized that the onset of speciation in sibling species from the Red Sea and the Indian Ocean, has been stipulated by allopatric divergence during Pleistocene isolation (Klausewitz 1989). If the two lineages of C. crenidens have taken the path towards evolution into separate species and if so, how far they have proceeded along it, cannot be said at the current state of research. From the point of view of morphological taxonomy, the single character in which specimens of C. crenidens from the Red Sea and the western Indian Ocean differed modally (i.e. the relative shorter pelvic fins in Red Sea specimens) is certainly not sufficient to recognize the two populations as separate species. The comparison of data taken from specimens in this study with that from previous ones (e.g. Iwatsuki and Maclaine 2013) showed that much more can be learned about variation of morphological characters in C. crenidens if a larger set of samples is analyzed. From a molecular taxonomical point of view, the reciprocal monophyly of specimens from different regions in the phylogenetic analysis prompts the interest in a more detailed analysis of the nature of the observed divergence. Next to single gene based methods that could be also applied with COI barcoding data (as e.g. provided by the General mixed Yule coalescent (GMYC) approach (Pons et al. 2006) or Automatic Barcode Gap Discovery (ABGD, Puillandre et al. 2012) more elaborate multi-gene coalescent-based approaches would be most promising in unraveling the state of evolutionary divergence in the two lineages in C. crenidens. However, at present we remain with the description of two separate and morphological almost identical evolutionary lineages of C. crenidens with presumably disjunct geographical distribution in the Red Sea and the western Indian Ocean, respectively.

Notes

Acknowledgments

Susanne Dorow and Jennifer Steppler are gratefully thanked for technical assistance at SMF and thanks are also due to Matthias Juhas and Stephanie Simon (SMF) and Fumiya Tanaka (MUFS) for assisting in molecular analyses. Sven Tränkner (SMF) kindly provided close-up images of specimens and we further acknowledge the Grunelius-Möllgaard Laboratory at SMF for lab support. We kindly appreciate the support of Roger Bills, Bafo Konqobe and Mzwandile Dwani (all SAIAB) by providing loans of specimens and colleagues at SAIAB are also thanked for donating tissue subsamples for molecular analyses. Shirleen Smith (USNM) is thanked for inspection of some specimens. Kent Carpenter and Millicent Sanciangco (both Old Dominion University) are thanked for their support. We thank to Gulab D. Khedkar (Paul Hebert Centre for DNA Barcoding and Biodiversity Studies, Dr. B.A. Marathwada University, Aurangabad, India) for permission to use his photograph and genetic data of the specimen from Gujarat, India. The scientific research cooperation between King Abdulaziz University (KAU), Faculty of Marine Sciences (FMS), Jeddah, Saudi Arabia, and the Senckenberg Research Institute (SRI), Frankfurt, Germany, in the framework of the Red Sea Biodiversity Project, during which the present material was collected, was funded by KAU GRANT NO. “I/1/432-DSR”. The authors acknowledge, with thanks, KAU and SRI for technical and financial support as well as Ali Al-Aidaroos, Mohsen Al Sofiyani and Mohamed M. Gabr (KAU), Fareed Krupp (SRI and Qatar Natural History Museum, Doha) for their help in the realization of the present study, and also Pirzada Jamal Siddiqui (PMNH) for financial support and sampling facilities in Pakistan.

Supplementary material

12526_2017_764_MOESM1_ESM.doc (71 kb)
Appendix 1 Information on specimens and sequences used in the maximum likelihood phylogenetic analysis of mitochondrial cytochrome c oxidase I (COI). (DOC 71 kb).

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Copyright information

© Senckenberg Gesellschaft für Naturforschung and Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Sergey V. Bogorodsky
    • 1
    • 2
  • Yukio Iwatsuki
    • 3
  • Shabir A. Amir
    • 4
    • 5
  • Ahmad O. Mal
    • 6
  • Tilman J. Alpermann
    • 1
  1. 1.Senckenberg Research Institute and Natural History Museum FrankfurtFrankfurt a.m.Germany
  2. 2.Station of NaturalistsOmskRussia
  3. 3.Department of Marine Biology and Environmental SciencesUniversity of MiyazakiMiyazakiJapan
  4. 4.Centre of Excellence in Marine BiologyUniversity of KarachiKarachiPakistan
  5. 5.Pakistan Museum of Natural HistoryIslamabadPakistan
  6. 6.Marine Biology Department, Faculty of Marine SciencesKing Abdulaziz UniversityJeddahSaudi Arabia

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