Diet composition and trophic interactions of nine fish species from Mocha water, southern Red Sea, Yemen

Regional Studies in Marine Science 29 (2019) 100693

Contents lists available at ScienceDirect

Regional Studies in Marine Science journal homepage: www.elsevier.com/locate/rsma

Diet composition and trophic interactions of nine fish species from Mocha water, southern Red Sea, Yemen N.A.M. Al Kamel, M.H. Kara

∗

Marine Bioresources Laboratory, Annaba University Badji Mokhtar, Algeria

article

info

Article history: Received 7 April 2018 Received in revised form 19 April 2019 Accepted 22 May 2019 Available online 24 May 2019 Keywords: Fish Food habits Diet overlap Mocha

a b s t r a c t Lethrinus lentjan, Lethrinus nebulosus, Lethrinus borbonicus, Lethrinus microdon, Sphyraena jello, Scomberomorus commerson, Euthynnus affinis, Carangoides chrysophrys and Caranx sexfasciatus are important fish of artisanal fishery of Mocha. In this area, no data is available on the biology and feeding ecology of these species. From May 2014 to June 2015, fish specimens (789) were sampled from the main fishing-landing site. Total length and total weight were measured and stomach contents were analyzed to evaluate the trophic interactions that exist between these species. Fish prey dominated in diets of all species except of L. nebulosus and L. lentjan, which mainly fed on mollusks. Based on diet similarity, four fish groups were identified: one includes L. microdon, C. chrysophrys, E. affinis and L. borbonicus, the other includes C. sexfasciatus, S. jello and S. commerson. Individually, L. lentjan and L. nebulosus form two separate groups. High dietary overlap was obtained among most species, associated with the dominance of small fish pelagic prey, perhaps because its abundance in the area, this implies a generalized and opportunistic utilization of resources. © 2019 Elsevier B.V. All rights reserved.

1. Introduction During the past years, the artisanal fishery expands in the Yemeni Red Sea fisheries dramatically. As a result of high income that fishermen have from the growing demand for fish and the government encouragement for investment in the fisheries, many coastal communities tended to work in fisheries, and fishing pressure is rabidly increasing. The number of fishermen and fishing boats have increased four times between 2000 and 2010 (Alabsi and Komatsu, 2014). The legal and illegal commercial fishing boats in the Red Sea fisheries is another issue regarding the increasing pressure on fisheries (PERSGA, 2002). The catch effort randomly increased without a clear management plans (Alabsi and Komatsu, 2014). In the Mocha as other Yemeni Red Sea areas, ecology and biology of coastal fishes are unavailable and the status of fish resources is nearly unknown. However, there are limited scientific literature describing the case of exploiting the Yemeni fisheries that includes Yemeni Red Sea fisheries (Alabsi and Komatsu, 2014; Tesfamichael et al., 2014, 2016). These studies indicated unsustainable exploitation. Brodie et al. (1999) concluded that the signs of heavy fishing of the top predator trophic layer are already apparent. According to the statistics of the Red Sea fisheries Authority′ s branch in Mocha, from 2010 to 2014, the landing consisted of shark, Scombridae, Lethrinidae, Serranidae, Lutjanidae, ∗ Corresponding author. E-mail address: [email protected] (M.H. Kara). https://doi.org/10.1016/j.rsma.2019.100693 2352-4855/© 2019 Elsevier B.V. All rights reserved.

Carangoidae, Haemulidae, Sphyraenidae, Rachycentridae, Sepiidae and bagha (a mixture of small pelagic fish include Clupeidae, Indian mackerel, Engraulidae and small Carangidae), its production has declined from 1805.1 in 2010 to 296.8 tons in 2014, and this may be a negative indicator of the exploitation of these species (Dalzell, 1996; Pauly, 1997; Hunt, 2003). Most of these predators are located at the top of the food chain and they are well known for their high sensitivity to overfishing (Jennings et al., 1999; Roberts, 1995; Coleman et al., 2000; Sadovy, 2001). Predators pressure is will not just have serious consequences for sustainability of fisheries and fish stock (Tsehaye, 2007), but can also have serious consequences on the community structure of marine environment as a whole (Jennings and Lock, 1996; Parsons, 1996; Dulvy et al., 2004). This suggests that the existing fisheries exploitation may be unsustainable, essential need for a more effective assessment and management. In the last few years, the Yemeni Ministry of Fish Wealth started to transfer responsibilities management of fisheries from the central level to the local level and has already established local fisheries authorities to be responsible for fisheries management at the local level (Alabsi and Komatsu, 2014). In this perspective, this study was focused on food habits of nine species of common and commercially important fishes from the main fishing landing sites of Mocha in south of the Yemeni Red Sea in order to assist local fisheries authorities in Mocha to establish ecosystem-based management of fisheries. Information about the diet of the some predatory fishes of the Yemeni Red Sea fisheries is available only from few studies

2

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693

Fig. 1. Map of Yemeni Red Sea area showing the location of Mocha city in the southern part of the Red Sea and the location of main landing-site on the Mocha coast.

in some other area of the Red Sea. Al-Zibdah and Odat (2007) compared between diet composition of Katsuwonus pelamis and E. affinis in the Gulf of Aqaba. Sabrah and El-Ganainy (2009) studied the stomach contents of Upeneus vittatus and U. tragula in the Gulf of Suez. Tesfamichael (2016) used Ecopath with Ecosim modeling tools in order to simulate trophic interactions in the Red Sea ecosystem with emphasis on its fisheries and many of diet data for the fish species obtained from other similar ecosystems or FishBase. Tsehaye (2007) prepared coral reef ecosystem model of the Eritrean Red Sea coast and many of the food data for the fish taken from similar marine environments. The main aims of this study are to get detailed information on the diet composition of some fish species in the Mocha’s water southern Yemini Red Sea and measure trophic overlap between these species. In addition, this study provides essential information for the creation of a first ecosystem-based management of species in these fisheries. 2. Material and methods 2.1. Study area The Mocha city is located in the southern coast of the Red Sea to the north of the Strait of Bab el Mandeb, between 13 ◦ 31′ and 13 ◦ 10′ N. Administratively, Mocha follows Taiz governorate and is about 94 km away from it, 170 km away from Hodeida and about 75 km away from the Strait of Bab el Mandeb (Fig. 1). With annual average rainfall ranging from 1 to 180 mm, the Red Sea area is generally arid (Edwards, 1987). Sea and air temperatures increase from north to south contrary to salinity. The average air temperature in the north is 17.5 ◦ C during August decreases to 15 ◦ C in January, while decreases from 37.5–47◦ C in August to 20–25◦ C during January in the south (DouAbul and Haddad, 1999). Salinity is around 40 psu in the north (26◦ N) at the gulfs of Suez and Aqaba, and decreases to 38 psu at 17◦ N, and 36.5 psu in the south of the Red Sea (12.5◦ N) (Edwards, 1987). 2.2. Sampling and data analysis From May 2014 to June 2015, 789 individuals representing the main nine species were sampled from the fish caught by the artisanal fishing gears, such as gillnets, handlining, surface long lines, trolling and cast net operated in the Red Sea and landed in the Mocha main landing site. Fish were identified according to Fischer and Bianchi (1984), measured (total length to the nearest

1 mm) and weighed (wet weight with 0.01 g precision). Stomachs were removed, put in plastic bags and stored in icebox. Samples were taken to the laboratory for analyzing stomachs contents the same day. The stomach content of 118 L. lentjan (Lacepède, 1802), 79 L. nebulosus (Forsskal, 1775), 174 L. borbonicus (Valenciennes, 1830), 69 L. microdon (Valenciennes, 1830), 74 S. jello (Cuvier, 1829), 63 S. commerson (Lacepède, 1800), 89 E. affinis (Cantor,1849), 64 C. chrysophrys (Cuvier, 1833) and 59 C. sexfasciatus (Quoy &Gaimard, 1825) were analyzed. Each prey item was identified to the lower taxonomic level possible by using appropriate taxonomic identification guides (Poore, 2004; Wolfgag, 1986; Fischer and Bianchi, 1984; Carpenter et al., 1997; Linder, 2010), counted and weighed (wet weight with 0.001 g precision). Unidentified prey items were stored in 75% ethanol in order to classify with the assistance of specialists. In order to know the importance of prey in the diet of species, the wet weight, number and frequency of occurrence of each prey item were recorded, collected for each species, then expressed as the percent by wet weight, number and frequency of occurrence (Hyslop, 1980; Windell and Bowen, 1978) as follows: Wi% = Wi/Wt ∗ 100 Ni% = Ni/Nt ∗ 100 Fi% = Fi/Ft ∗ 100 where Wi% is percent by wet weight of prey i, Wi is the total wet weight of prey i, Wt is the total wet weight of prey, Ni% is percent by number of prey i, Ni is the total number of prey i, Nt is the total number of all preys, Fi% is percent by frequency of occurrence of prey i, Fi is the frequency of occurrence of prey i, Ft is the total number of full stomachs. The wet weight of each prey item were collected for each month independently and expressed as the percent (W%), to know the importance of prey for each species among study months. Cluster analysis within the PRIMER5 software package (Clarke and Gorley, 2001) was used in order to group fish species (Clarke and Warwick, 1994) based on food similarity (by wet weight). Diet data re-assembled at the family level, and Bray–Curtis similarity index was used to the computation of the matrix of similarity between species. The similarity matrix was treated by hierarchical agglomerative cluster/group average linking method to get a dendrogram that illustrates the fish groups. The interpretation grouping within the graph was determined by an arbitrary cut off value for dissimilarity (Quinn and Keogh, 2002). Also, similarity matrix was treated by non-metric, multi-dimensional scaling (MDS) to confirm the result of grouping. Similarity analysis (ANOSIM/one way) (Clarke and Warwick, 1994) was employed

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693

3

Fig. 2. Length frequency distribution of nine fish species sampled in Mocha coast southern Red Sea in Yemen.

to test the hypothesis of no differences between the fish groups. This test compares the average of rank similarities between and within groups (value close to 1 indicate a significant difference between the groups then within group and the value close to 0 indicate no difference) (Clarke and Gorley, 2001). The similarity percentage (SIMPER) analysis (Clarke and Warwick, 1994) was used to identify the prey responsible for particular aspects (i.e. average dietary similarities) of the multivariate structure found in the Bray–Curtis similarity matrix (Clarke and Gorley, 2001). Overlap index was used to measure the amount of food resources overlap between different species. It is sometimes used to infer competition, however, the existence of food overlap does

not necessarily cause competition between species, may be due to the abundance of food resources (Cabral et al., 2002). Wet weight for items prey by Morisita–Horn index was used to measure trophic overlap between fish species: Chi = 2(Σ Phk ∗ Pik )/(Σ P2 hk + P2 ik ) where Chi is the overlap between species h and i, Phk is percentage of resource k of the total food used by species h, Pik is percentage of resource k of the total food used by species i (Hall et al., 1990). Food overlap values ranging from 0 when no food is shared, to 1 when there is the same proportional use of all food resource. Although there are no critical levels with which overlap can be

4

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693 Table 1 List of fish species collected form Mocha coast in Yemen for diet composition study. Family

Species

Number of individuals measured

Range of total length (cm)

Range of weight (kg)

Number of Full stomach samples with full % stomachs

Lethrinidae

L. L. L. L.

118 79 174 69

22.0 23.0 18.0 26.0

0.13 – 0.73 0.17– 2.06 0.09 – 0.24 0.18 – 2.61

54 40 61 32

45.76 50.63 35.06 46.38

Sphyraenidae

S. jello

74

46.0 – 119.0

0.53 – 5.46

37

50.00

Scombridae

S. commerson E. affinis

63 89

57.0 – 129.0 43.0 – 80.0

1.02 – 15.0 1.36 – 5.46

41 40

65.08 44.94

Carangoidae

C. chrysophrys C. sexfasciatus

64 59

31.0 – 63.0 49.0 – 79.0

0.43 – 2.56 1.42 – 3.89

39 34

60.94 57.63

lentjan nebulosus borbonicus microdon

– – – –

41.0 57.0 25.0 60.0

Fig. 3. Food items of the nine studied fish species from Mocka coast in Yemen expressed as percentage of wet weight (W%), number (N%) and frequency of occurrence (F%).

compared (Cabral et al., 2002; Wallace, 1981; Zaret and Rand, 1971) suggested that if the value of the overlap equals to or more than 0.60, then it should be of a biological significance. 3. Results 3.1. Diet composition Fig. 2 shows size frequency distribution of each sampled fish species. Table 1 shows the percentages of full stomachs for each studied species and summarizes the ranges of their total length (TL) and weight (W). Ninety-nine prey taxa were found in the stomachs of the 9 species, including 38 mollusks, 30 fish, 13 echinoderms, 17 crustaceans and one prey belonging to polycheates (Table 2). Fig. 3 summarizes the preferential prey items for each species. Fish prey dominated (by wet weight, number and occurrence) in the diet of all fish species except L. nebulosus and L. lentjan where Molluscs occupy the first position. Echinoderms were important food for L. nebulosus and less important for L. lentjan. Crustaceans were important prey for L. borbonicus, L. lentjan and L. nebulosus. They were important by frequency of occurrence for C. chrysophrys and E. affinis with 20.51% and 15.00% respectively. L. lentjan consume a wide range of prey representing five groups: mollusks, crustaceans, fish, echinoderms and polycheates (Table 3). Mollusks and crustaceans were the most important prey and predominant in all study months except August (Table 4). Fish were the other important prey, but appears only in January, June and August in large specimens (more than 28 cm). Mollusks were the dominant prey for L. nebulosus followed by

echinoderms and crustaceans (Table 3). Mollusks included 18 different prey items represent three classes (gastropods, bivalves and Polyplacophora) and echinoderms category included six prey represent four mainly groups (sea urchins, star fish, brittle star and sea cucumber). Within mollusks, bivalves were the main food (22.11% W). Fish prey was secondary food with 10.00% by frequency of occurrence, found in the stomach of specimens larger than 41 cm T.L (Table 4). In L. borbonicus, fish prey dominated by wet weight (63.39%) and by frequency of occurrence (45.90%) (Table 3). Small pelagic fish (Clupeidae) were the most important and formed the largest proportion in the diet during December and January (Table 4). Food of L. microdon consists of three categories: fish, crustaceans and polycheates (Table 3). Fish item formed 93.42% by wet weight, 80.77% by number and 90.63% by occurrence. Clupeidae were the dominant prey during January (77.15% W), June (84.77% W), August (74.21% W) and December (69.52% W) (Table 4). Fish prey also dominated in the diet of S. jello (Table 3). Clupeidae, Engraulidae and Mugilidae are the most important within fish. Small pelagic fish formed larger proportion among the diet in January, June and December (Table 4). Fish prey is the only food of S. commerson. Clupeidae, Carangoidae, Engraulidae and Scombridae were the most important (Table 3). In E. affinis, fish is the main food (Table 3). Clupeidae and Engraulidae dominated. Clupeidae and Engraulidae formed the highest of percentage of the diet of E. affinis in June, August and December (Table 4). In C. chrysophrys, fish is the main prey. Clupeidae was the most important (Table 3) and during June, August and December, this prey formed the highest percentage (Table 4). Crustaceans were another important prey items in terms of occurrence (20.51%). C. sexfasciatus mainly

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693

5

Table 2 List of prey found in the stomachs of nine studied fish species from Mocha coast southern Red Sea in Yemen. Prey Fish

Crustaceans

Mollusks

Echinoderms

Polycheates

Fish (Unident.) Clupeidae Clupeidae (Unident.) Sardinella sp. Heerkoltsichthys sp. Sardinella sirm Heerkoltschthys punctatus Scombridae Scombridae (Unident.) Rastrelliger sp. Mugilidae Mugilidae (Unident.) Liza sp. Mullidae Mullidae (Unident.) Parupeneus sp. Engraulidae Engraulidae (Unident.) Stolophorus sp. Stolophorus puctifer Tryssa setirostris Lutjanidae Lutjanus sp. Lethrinidae Lethrinidae (Unident.) Lethrinus sp Carangoidae Carangoidae (Unident.) Trachurs indicus Decapterus sp. Sphyraenidae Sphyraena sp. Leiognathidae Leiognathidae (Unident.) Leiognathus sp. Secutor sp. Holcentridae Myripristis murdjan Balistidae Balistidae (Unident.) Odonus niger Beleniidae Beleniidae (Unident)

Crustaceans (Unident.)

Mollusks (Unident.) Gastropoda Trochidae Agagus sp. Agagus stellamaris Cypraeidae Cypraea caurica Neritidae Nerita sp. Nerita sanguinolenta Muricidae Muricidae (Unident.) Calyptraeidae Calyptraeidae (Unident.) Calyptraea sp. Crepidula sp. Nassariidae Nassariidae (Unident.) Nassarius isseli Bullidae Bulla sp. Strombridae Strombus sp. Bivalvia Bivalvia (Unident.) Cardiidae Cardiidae (Unident.) Acrosterigma sp. Parvicardium sp. Veneridae Veneridae (Unident.) Tirela sp. Tirela ponderos Timoclea sp. Myidae Myidae (Unident.) Pholadidae Pholadidae (Unident.) Telinidae Telinidae (Unident.) Tellina palatum Tellina sp. Tellina pinguis Mactridae Mactridae (Unident.) Petriidae Pteria sp. Mytilidae Mytilidae (Unident.) Modiolus sp. Cultellidae Cultellidae (Unident.) Arcidae Arca sp. Pinnidae Pinna sp. Chiton Polyplacophora Chitonidae Chiton sp. Ischnochitonidae Ischnochiton sp. Cephalopoda Sepiidae Sepia sp.

Star fish Asteroidae Asteroidae (Unident.) Brittlestar Ophiuroidae Ophiuroidae (Unident.) Comatulidae Comatulidae (Unident.) Amphiuridae Amphiura sp.

Polycheates (Unident.)

Isopodae Isopodae (unident.) Cirolanidae Excirolana sp. Crabs Crabs (Unident.) Portunidae Portunidae (unident.) Portunus sp. Scylla serrata Xanthidae Capilius sp. Leptodius sp. Leuucosiidae Leucosia anantum Nursia sp. Ocypodidae Uca sp. Ocypoda sp. Macrophthalmus depressus Grapsidae Perisesarma sp. Shrimps Penaeidae Penaeidae (Unident.) Penaeus smeisulcatus

feed on fish prey which dominated by wet weight (98.30%), by number (94.92%) and by frequency of occurrence (102.94%) (Table 3). Clupeidae was the first (32.93% W, 38.24% F) followed by Scombridae (16.54% W, 17.65% F), Carangoidae (12.30% W) and Mugilidae (9.17% W). Clupeidae were more present in June, August and December (Table 4).

Sea urchins Echinometridae Echinometridae (Unident.) Schizasteridae Schizasteridae (Unident.) Schizaster sp. Parasaleniidae Parasaleniidae (Unident.) Parasalenia sp. Clypeasteridae Clypeasteridae (Unident.) Clypeaster amplificatus Diadematidae Diadematidae (Unident.) Sea cucumber Holothuridae Holothuridae (Unident.)

3.2. Cluster analysis Cluster dendrogram shows that the nine fish species divided into four groups based on food similarity at approximately 35% (Bray–Curtis similarity) (Fig. 4). First group consists of four predators (L. microdon, C. chrysophrys, E. affinis and L. borbonicus).

6

Table 3 Diet composition of the nine studied fish species from Mocha water in Yemen, expressed as present by wet weight (W%), number (N%), and frequency of occurrence (F%). Index

L. lentjan W%

L. nebulasus F%

W%

L. borbonicus

N%

F%

W%

N%

L. microdon F%

W%

N%

S. jello F%

W%

S. commerson N%

F%

E. affinis

W%

N%

F%

W%

N%

C. chrysophrys F%

W%

N%

C. sexfasciatus F%

W%

N%

F%

16.60 7.84

14.81 5.62

1.14

5.00

22.82 19.75 26.23 10.83 17.31 25.00 10.11 11.94 13.51

9.28

10.53

12.20

8.12

10.84 17.50

17.65 11.84 17.95 14.70 16.95 23.53

6.88 . . . . . . . . . . . . 23.48 2.87

1.96 . . . . . . . . . . . . 9.80 2.94

3.70 . . . . . . . . . . . . 18.52 3.70

. . . . . 6.76 5.70 . . . . . . 18.08 .

. . . . . 1.14 .57 . . . . . . 2.86 .

. . . . . 2.50 2.50 . . . . . . 10.00 .

24.95 8.65 . . . 6.97 . . . . . . . 63.39 .

8.64 3.70 . . . 2.47 . . . . . . . 34.57 .

11.48 4.92 . . . 3.28 . . . . . . . 45.90 .

49.18 9.18 6.31 . . . . 17.92 . . . . . 93.42 .

44.23 9.62 7.69 . . . . 1.92 . . . . . 80.77 .

46.88 9.38 6.25 . . . . 3.13 . . . . . 90.63 .

32.41 9.53 13.56 9.98 9.00 4.55 . . 4.18 . . . . 93.32 .

47.76 13.43 7.46 8.96 2.99 2.99 . . 2.99 . . . . 98.51 .

56.76 13.51 13.51 8.11 5.41 2.70 . . 2.70 . . . . 116.22 .

30.76 14.33 8.78 11.92 21.36 . . . . 3.56 . . . 100.00 .

40.79 14.47 11.84 10.53 10.53 . . . . 1.32 . . . 100.00 .

31.71 17.07 9.76 12.20 17.07 . . . . 2.44 . . . 102.44 .

44.20 22.53 . 8.10 . . . . 1.90 . 1.74 2.05 . 88.65 .

34.94 28.92 . 6.02 . . . . 1.20 . 1.20 1.20 . 84.34 .

45.00 27.50 . 10.00 . . . . 2.50 . 2.50 2.50 . 107.50 .

58.45 8.62 . . . . . 7.50 . . . . 4.35 96.58 .

52.63 9.21 . . . . . 1.32 . . . . 1.32 76.32 .

51.28 12.82 . . . . . 2.56 . . . . 2.56 87.18 .

32.93 . 9.17 16.54 12.30 . . . 6.71 . . . 5.95 98.30 .

45.76 . 10.17 10.17 5.08 . . . 5.08 . . . 1.69 94.92 .

38.24 . 8.82 17.65 8.82 . . . 2.94 . . . 2.94 102.94 .

1.45 19.97 2.99 27.28

2.94 23.53 1.96 31.37

1.85 31.48 3.70 40.73

2.05 14.47 . 16.53

1.14 11.43 . 12.57

2.50 17.50 . 20.00

. 18.66 3.49 22.15

. 29.63 3.70 33.33

. 31.15 4.92 36.07

. 3.46 . 3.46

. 15.38 . 15.38

. 9.38 . 9.38

. . . .

. . . .

. . . .

. . . .

. . . .

. . . .

0.21 0.92 0.61 1.73

1.20 9.64 2.41 13.25

2.50 7.50 5.00 15.00

. 2.14 0.31 2.45

. 21.05 1.32 22.37

. 17.95 2.56 20.51

. 1.70 . 1.70

. 5.08 . 5.08

. 5.88 . 5.88

.

.

.

4.58

.57

2.50

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

.

10.17 25.29 3.16 . 38.61

11.76 38.24 1.96 . 51.96

12.96 25.93 3.70 . 42.59

8.51 22.11 5.62 . 40.82

13.71 64.00 1.71 . 80.00

15.00 32.50 7.50 . 57.50

3.07 5.64 . . 8.70

6.17 19.75 . . 25.93

6.56 9.84 . . 16.39

. . . . .

. . . . .

. . . . .

. . . 6.68 6.68

. . . 1.49 1.49

. . . 2.70 2.70

. . . . .

. . . . .

. . . . .

. . . 9.62 9.62

. . . 2.41 2.41

. . . 5.00 5.00

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

0.80 0.80 3.26 . 4.86

0.98 0.98 3.92 . 5.88

1.85 1.85 7.41 . 11.11

4.85 3.23 14.27 2.23 24.57

.57 .57 2.86 .57 4.57

2.50 2.50 12.50 2.50 20.00

. .77 1.43 . 2.20

. 1.23 1.23 . 2.47

. 1.64 1.64 . 3.28

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

. . . . .

5.76

0.98

1.85

.

.

.

3.56

3.70

1.64

3.12

3.85

3.13

.

.

.

.

.

.

.

.

.

0.97

1.32

2.56

.

.

.

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693

Fish (Unident) Clupeidae Engraulidae Mugilidae Scombridae Carangoidae Mullidae Lutjanidae Lethrinidae Leiognathidae Sphyraenidae Beleniidae Holcentridae Balistidae Fish (total) Crustaceans (Unident.) Isopodae Crabs Shrimp Crustaceans (total) Mollusks (Unident.) Gastroboda Bivalvia Chiton Sepia Mollusks (total) Star fish Brittlestar Sea urchins Sea cucumber Echinoderms (total) Polycheates

N%

Lutjanidae

Mullidea

Leiognathidae

Sphyraenidae

Holcentridae

Beleniidae

Balistidae Crustaceans

Mollusks

Echinoderms

Polycheates

E.affinis

Lethrinidae

S.commerson

Prey items

Carangoidea

S. jello

Range of total length (cm) of samples with mollusks & Crustacean in stomach

Scombridae

L. microdon

Range of total length (cm) of sample with Echinoderm prey in stomach

Mugilidae

L. borbonicus

Range of total length (cm) of sample with fish prey in stomach

Engraulidea

L. nebulasus

Number of samples with full stomach

January March May June August December January March May June August December January March May December January March June August November December January March May June November December January March May June August November December March May June August November December

10 17 4 6 9 8 5 7 8 5 6 9 6 7 26 22 3 3 5 6 11 4 5 3 7 10 6 6 3 7 9 7 5 5 5 4 8 10 5 3 10

31 – – 29–41 29–35 – 42 – 53 – 43 – 22–24 23 22.5–24 22–25 30–43 31–34 34–48 31–60 30–42 31–48 47–54 61–95 59–119 46–69 47–81 51–101 57–71 57–104 69–108 69–96 58–76 68–82 62–129 48–62 53–66 51–70 52–65 54–69 45–73

33–34 32–36 35 – – – 41–42 – 44 36 37–45 39–41 – 23.5 22 – – – – – – – – – – – – – – – – – – – – – – – – – –

23–29 24–29 25–27 24–30 25–29 22–29 27–35 24–35 24–33 26–31 29–33 23–31 19.5 20–21 19–21 19–21 30–35 26 – – – – – – 95 – – – – – – – – – – 48 51–60 – – – –

16.54 – – 39.15 43.64 – 18.28 – – – 18.61 – 32.76 11.96 11.93 29.96 – – 15.23 – 43.08 – – 10.02 23.31 – – 14.98 – 28.70 17.98 – – 13.04 – 20.09 15.55 – 8.64 28.07 4.27

– – – – 34.57 – – – – – – – 57.50 – 3.09 37.35 77.15 10.66 84.77 74.21 25.33 63.00 45.21 19.45 5.25 44.79 27.28 66.93 44.82 4.98 7.28 42.31 34.02 32.39 55.06 21.81 11.56 63.04 57.50 – 50.01

– – – – – – – – – – – – – – – 17.77 – – – 25.79 – 37.00 54.79 – 3.09 – 15.67 18.10 37.16 – 5.10 30.14 24.07 – 16.88 – 6.13 16.53 33.86 46.39 32.31

– – – – – – – – – – – – – – – – – – – – 31.60 – – 36.51 7.71 15.02 27.38 – – 15.64 16.13 – 16.55 – 9.10 – – – – – –

– – – – – – – – – – – – – – – – – – – – – – – – 5.11 20.45 29.67 – 18.02 – – 27.55 25.37 – 18.96 – – 20.43 – 25.53 13.41

– – – – – – – – – – – – – – – – – – – – – – – – 14.74 19.74 – – – 26.28 53.51 – – 54.56 – – – – – – –

– – – – – – – – – – – – – – – – – 72.09 – – – – – – – – – – – – – – – – – – – – – – –

– – – – – – – – 19.81 – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – –

– – – – – – – – 23.48 – – – – – 22.77 – – – – – – – – – 16.52 – – – – – – – – – – – – – – – –

– – – – – – – – – – – – – – – – – – – – – – – 34.02 – – – – – – – – – – – – 8.68 – – – –

– – – – – – – – – – – – – – – – – – – – – – – – – – – – – 24.40 – – – – – – – – – – –

– – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – 9.37 – – – –

– – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – 41.77 – – – – –

– – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – – –

45.70 28.51 69.81 60.85 21.79 41.88 5.24 58.86 36.51 54.11 47.43 51.71 – 20.78 18.28 1.86 – – – – – – – – 24.28 – – – – – – – – – – – 43.91 – – – –

8.88 8.98 16.34 – – – 35.19 – 9.53 45.89 33.96 34.03 – 13.48 2.53 – – – – – – – – – – – – – – – – – – – – – – – – – –

– – – – – 35.94 – – – – – – – 33.63 – – – 12.56 – – – – – – – – – – – – – – – – – – – – – – –

28.88 62.51 13.85 – – 22.18 41.29 41.14 10.68 – – 14.26 9.74 20.15 41.40 13.06 22.85 4.69 – – – – – – – – – – – – – – – – – 16.33 4.80 – – – –

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693

L. lentjan

Month

Clupeidae

Species

Fish (Unident.)

Table 4 Monthly variation of the importance for prey items (by wet weight) founded in the diets of nine fish species from Mocha coast southern Red Sea in Yemen.

(continued on next page) 7

8

27.80 29.32 62.79 81.44 35.71 100.0 – – 58.50 50.45 – 43.00

– – 14.73 18.56 – – – – – – – –

– – – – – – – 24.42 – 27.89 – –

– – – – – – – – 41.50 18.63 – 19.22

– – – – – – 33.77 – – – 22.38 25.40

41.15 – – – – – – – – – – –

– – – – – – – – – – – –

– – – – – – – – – – – –

– – – – – – – – – – 38.76 –

– – – – – – – – – – – –

Polycheates

27.78 56.20 22.48 – 19.16 – 18.36 46.92 – 3.03 38.86 12.38

Echinoderms

Lutjanidae

45–57 31–32 – – 53–54 – – 69–70 – – – –

Mollusks

Lethrinidae

– – – – – – – – – – – –

Crustaceans

Carangoidea

32–59 55–63 44–61 31–62 47–54 52–56 51–79 61–70 51–73 55–78 52–76 50–76

Balistidae

Scombridae

7 7 9 10 4 2 3 3 7 9 5 7

Holcentridae

Mugilidae

March May June August November December March May June August November December

Beleniidae

Prey items

Sphyraenidae

Range of total length (cm) of samples with mollusks & Crustacean in stomach

Mullidea

Range of total length (cm) of sample with Echinoderm prey in stomach

Leiognathidae

Range of total length (cm) of sample with fish prey in stomach

Engraulidea

C.sexfasciatus

Number of samples with full stomach

Clupeidae

C.chrysophrys

Month

Fish (Unident.)

Species

– – – – – – – – – – – –

– – – – – – – – – – – –

– – – – 33.60 – 47.87 – – – – –

3.26 14.48 – – 4.03 – – 28.66 – – – –

– – – – – – – – – – – –

– – – – – – – – – – – –

– – – – 7.51 – – – – – – –

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693

Table 4 (continued).

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693

According to SIMPER analysis, preys of Clupeidae and Engraulidae were most contributory in the average of food similarity within this group. Within group, dietary similarity between C. chrysophrys and L. microdon is the highest (78.53%) followed by the similarity between C. chrysophrys and L. microdon as one group with E. affinis (61.16%) and between L. borbonicus with C. chrysophrys, L. microdon and E. affinis as one group (54.11%). The second group including C. sexfasciatus, S. jello and S. commerson. Within this group, Clupeidae, Scombridae, Mugilidae and Carangoidea were species responsible in the average of food similarity. Similarity between S. jello with S. commerson is 79.51%, and between S. jello and S. commerson as one group with C. sexfasciatus is 72.98%. Third (L. lentjan) and forth (L. nebulasus) group consist of only one species. The cluster dendrogram proved that diet of L. lentjan and L. nebulosus was different from the other predators, but food of L. nebulosus was most different. The similarity between L. nebulosus and other groups was very low (5.37%). By using MDS, the division of nine fish species in four groups according to diet similarity is confirmed. Again, L. microdon, C. chrysophrys, E. affinis and L. borbonicus appeared clearly closed. C. sexfasciatus, S. jello and S. commerson were also close. L. lentjan separated from the rest of predators but L. nebulosus was more isolated from the other species (Fig. 5). A value of R (0.926), which was obtained from the similarity analysis (ANOSIM/one way) supports the results of the classification by using cluster analysis and coordination by MDS, indicating that there are significant differences in diet composition between the groups (p = 0.2%). 3.3. Trophic overlap Morisita–Horn index shows the existence of high diet overlap between fish species except for L. nebulosus (Table 5). The highest overlap was between L. microdon and C. chrysophrys and between C. sexfasciatus and S. jello. The food overlap was greater than 0.80 but less than 0.90 between C. sexfasciatus and S. commerson (sharing in Clupeidae, Scombridae and Mugilidae) and for each pair of L. borbonicus, L. microdon and E. affinis (sharing in Clupeidae and Engraulidae) and for each pair of S. jello, L. borbonicus, and E. affinis (sharing in Clupeidae and Engraulidae). A considerable high food overlap was between C. sexfasciatus with each of L. borbonicus, L. microdon, C. chrysophrys and E. affinis as well as between S. commerson and with each of L. microdon, C. chrysophrys and L. borbonicus also between L. borbonicus and L. lentjan. The overlap between L. lentjan with each of S. jello, L. microdon, C. chrysophrys, E. affinis, C. sexfasciatus and S. commerson was close to a considerable overlap. L. nebulosus has less overlap with other predators. 4. Discussion This study, for the first time, covers the food components of some commercially important fish found at the main landing site in Mocha city, south of the Yemeni Red Sea and highlights the monthly changes for food habits for these predatory species during study period. Another commercial fish such as Trachurus longimanus (Norman, 1935), Scomberoides commersonianus (Lacepè, 1801), Caranx ignobilis (Forsskål, 1775), Elagatis bipinnulatus (Quoy & Gaimard, 1825), Diagramma pictum (Thunberg, 1792) and Epinephelus polylepis (Randall &Heemstra, 1991) were less important in size and production and most of the times their were sampled of these species with empty stomachs. This can be interpreted as an initial indication of overfishing pressure on fish stocks in these fisheries. In L. lentjan, benthic invertebrates (mollusks, 38.61% W and crustaceans, 27.28% W) represented the most important prey as found by Toor (1964), Salini et al. (1994) and Kulbicki et al.

9

(2005). This could be related to the predator’s behavior, body shape and jaws morphology. In fact, L. lentjan is benthic feeding (Toor, 1964), and inhabits sandy bottom in coastal, coral reef waters and deep lagoons. It has deep body forms and lateral rounded teeth in jaws including distinct molars (Carpenter and Allen, 1989; Fischer and Bianchi, 1984) allows the processing of a wide range of benthic invertebrates including soft and hardshelled such as mollusks and crustaceans (Carpenter, 1996; Costa and Cataudella, 2007). Fish prey are found in large specimens (more than 28 cm) as reported by Toor (1964) and Kulbicki et al. (2005). For L. nebulous, mollusks (40.82% W), echinoderms (24.57 W) and crustaceans (16.53% W) were mainly food as is the case in New Caledonia (Kulbicki et al., 2005) and in the Barrier great Reef in Australia (Walker, 1978). The nocturnal activity of this carnivorous predator (Chabanet and Durville, 2005) and its prey (Kulbicki et al., 2005) explains this specialization. The presence of lateral rounded teeth in its jaws with distinct molars often with tubercles (Carpenter and Allen, 1989; Fischer and Bianchi, 1984) enables this fish to process a wide range of benthic invertebrates including both soft and hard-shelled preys (Carpenter, 1996; Costa and Cataudella, 2007). As indicated by Ali et al. (2016), echinoderms are found in stomachs of specimens larger than 35 cm TL while mollusks and crustaceans in small size specimens (less than 38 cm total TL). The absence of mollusks and crustaceans in the largest specimens is perhaps due to a low nutritional value, which will not meet the energy needed to consume large quantities of them (Kulbicki et al., 2005). Fish prey was secondary food, found in the stomach of specimens larger than 41 cm TL as found by Kulbicki et al. (2005) and Egretaud (1992). In L. borbonicus, fish prey predominates and Clupeidae are more important mainly in December and January because of the abundance of small pelagic fish during these months in the southern part of the Red Sea. Benthic invertebrates (crustaceans, mollusks) come in second rank, which confirms the findings of Ali et al. (2016). Carpenter and Allen (1989) and Tharwat and AlGaber (2006) stated that L. borbonicus feeds mainly on mollusks, crustaceans and echinoderms. For L. microdon, fish prey (especially Clupeidae) predominates to 93.42% by wet weight. It has an elongated body form and conical teeth (Carpenter and Allen, 1989) give an advantage to eat fish prey (Kulbicki et al., 2005). This result is confirmed by Ali et al. (2016), but does not correspond to Fischer and Bianchi (1984) who stated that L. microdon feeds on crustaceans, mollusks and small fish, nor with Carpenter and Allen (1989) who stated that L. microdon mainly feeds on fish, crustaceans and polycheates. Fish prey dominated in the diet of S. jelloas is the case on the coasts of Malaysia (Bachok et al., 2004), Australia (Baker and Sheaves, 2005) and India (Mohanraj and Prabhu, 2012). Clupeidae are the first prey among fish mainly in January, June and December. Hosseini et al. (2009) found that Clupeidae (Tenualosa ilisha) and Mugilidae (Liza subviridis) are the majority in the diet of this species. Jeyaseelan (1998) stated that S. jello is a carnivorous predator feed on fish and squid. Diet of S. commerson only consists of fish prey. Clupeidae, Carangoidae, Engraulidae and Scombridae (Rastrelliger sp.) were the main prey. The same prey in the diet of S. commersonis found by Bachok et al. (2004) in the east coast of Malaysia, by Bakhoum (2007) in Egyptian Mediterranean coast and by Godcharles and Murphy (1986) in south Florida. In Salmon Islands, Blaber et al. (1990) found that fish prey dominated (99.9%) in the diet of S. commerson where Mugilidae, Clupeidae (sardinella spp.), Carangoidae and Engraulidae (Stolophorus spp.) consisted of about 50% followed by unidentified fish (46.37%). For E. affinis, fish prey is the main food and Clupeidae, Engraulidae and Scombridae (Rastrelliger sp.) represented an important

10

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693

Fig. 4. Bray–Curtis similarity dendrogram resulting from cluster analysis implemented on diet composition expressed as percent of wet weight (W%) (at family level) for the nine fish species from the Mocha water southern Red Sea in Yemen.

Fig. 5. Non-metric, multi-dimensional scaling (MDS) plot for nine fish species from the Mocha water in Yemen based on diet similarity (by wet weight (W%) at family level) Stress = 0.01. Table 5 Morisita–Horn index values of food overlap between the nine fish species caught by artisanal fishers from the Mocha coast in Yemen. Species L. L. L. L. S. S. E. C. C.

lentjan nebulosus borbonicus microdon jello commerson affinis chrysophrys chrysophrys

L. lentjan

L. L. L. S. jello S. E. nebulosus borbonicus microdon commerson affinis

C. chrysophrys

0.12 0.71 0.57 0.58 0.49 0.55 0.54 0.54

0.14 0.01 0.04 0.00 0.00 0.00 0.00

0.71

0.82 0.82 0.73 0.87 0.80 0.68

0.79 0.72 0.87 0.95 0.72

prey, which consumed with large percentage in June, August and December. This may be due to the increasing abundance of this prey in the Mocha fisheries during these months (personal observation). Clupeidae and Engraulidae formed 87.39% of the food of this species in Salmon Islands (Blaber et al., 1990) while Anchovy and Indian mackerel are the essential prey in the east coast of Malaysia (Bachok et al., 2004). E. affinisalso consume crustaceans and squid, which agrees with the results of Al-Zibdah and Odat (2007). For C. chrysophrys also, fish prey (Clupeidae in particular) dominates, especially in June, August and December. Fish formed 62% of the food of this species in New Caledonia (Kulbicki et al.,

0.92 0.86 0.75 0.91

0.80 0.69 0.88

0.89 0.74

C. chrysophrys

2005) and 92.4% in the Gulf of Carpentaria in Australia (Salini et al., 1994). Clupeidae, Engraulidae and Atherinidae represented 73% of the diet consumed by C. chrysophrysin Fiji Island (Blaber et al., 1993). With 98.3% by wet weight, C. sexfasciatus is essentially piscivorous fish as already found by Salini et al. (1994), Durville et al. (2003), Bachok et al. (2004) and Baker and Sheaves (2005). In Kuchierabu-jima Island - southern Japanese, Takeuche et al. (2007) found that small pelagic fish and crustaceans occurred respectively in about 58% and 63% in the stomachs of C. sexfasciatus. The important occurrence of crustaceans in this case may be due to the relatively important number of specimens with small size

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693

(11.8 cm–23.0 cm). Indeed, Blaber and Cyrus (1983) found that individuals smaller than 20 cm TL mainly feed on crustaceans, while larger ones entirely feed on fish. Fish prey dominated (by wet weight, number and occurrence) in the diet of most studied species in Mocha region. Clupeidae was the principal prey, forming the highest percentage in the diet of L. barbonicus, L. microdon, S. jello, S. commerson, E. affinis, C. chrysophrys and C. sexfasciatus during June, Augusts, December and January. This may be due to abundance of this prey during these months in the Mocha fisheries. Indeed, near the Gulf of Aden, nutrients-rich water bringing to photic zone into water column during southwest monsoon winds which blow from June to September (period of upwelling event) and northeast monsoon winds occur from December to February (period of mixing vertical). This leading to increase primary production in the region (Banse, 1987; De Souza et al., 1996; Madhupratap et al., 1996; Schott et al., 1990) and a boom in phytoplankton and zooplankton in these times. The southern part of Red Sea receives a lot of this plankton by flow of rich-water from Gulf of Aden through Strait of Bab el-Mandeb (away from Mocha 75 km) (Halim, 1969), providing suitable surrounding for the formation of big biomass of small pelagic fish. Unlike other prey, the percentage of Clupeidae and Engraulidae has decreased in March and May perhaps because the availability of small pelagic fish is lower during these months. This may be a sign that species changed their patterns diet to most available preys. This opportunistic behavior in utilization dietary resources aims to reduce the competition between species and facilitate coexistence within the same zone (Anderson et al., 1981). Fish species may feed at different levels in the food chain at various stages of their life cycle. Fish prey increasingly important with the increased of the size of L. lentjan, L. borbonicus and L. nebulosus unlike crustaceans and mollusks, which highlights a large percentage in the diet of small sizes of these species. Many of previous studies investigate changes of consumption of prey item with increase predator’s size, agreement with this study (Toor, 1964; Blaber and Cyrus, 1983; Egretaud, 1992; Kulbicki et al., 2005; Ali et al., 2016). The favorite fish food is very complex and affected by many factors such as the abundance of prey, the energy content of the prey, the size of prey and the changes in seasons (Hart and Ison, 1991, Stergiou and Fourtouni, 1991, Brewer and Warburton, 1992, Barry and Ehret, 1993 cited in Bachok et al., 2004). Cluster analysis shows that four groups formed according to dietary similarity (at family level by wet weight). The dietary breakaway between groups is due to differences in food components, as well as differences of Percentages of sharing prey consumed by fish. This partition may be related to feeding behaviors, prey species availability, habitat, size of prey consumed and predator morphology (Platell and Potter, 2001). Group 1 consists of L. microdon, C. chrysophrys, E. affinis and L. borbonicus. SIMPER analysis shows that the average food similarity for this group is 60.35% based on their share in Clupeidae and Engraulidae. Inside group, the variation of similarity between species is related to the differences due to the proportion of consumed Clupiedae and Engraulidae, in addition to the difference in other prey. Group two has average dietary similarity of 73.30%, including three species (S. jello, S. commerson and C. sexfasciatus) based on similarity consumption of Clupeidae, Scombridae, Mugilidae and Carangoidea. Group three and four included one species. Group 3 (L. lentjan) was more close to group 1 and group 2 than Group 4 (L. nebulasus). L. lentjan consume Clupeidea but with very low proportion in comparison with group 1, 2. L. nebulosus has less similarity with other groups (5.37%). In fact, L. nebulosus feeds on benthic fish (Mullidae, Lutjanidae) and a wide range of benthic invertebrate (crustaceans, mollusks and echinoderms).

11

High dietary overlap exists between the studied species. It is associated with high percentages of small pelagic fish (especially Clupeidae) in the diet. This overlap does not necessarily lead to competition between predators, may be due to the abundance of prey (Cabral et al., 2002). The abundance of dietary resources emphasizes a generalized and opportunistic utilization of these resources (Beyst et al., 1999; Lasiak and Mclachlan, 1987). In this regard, although L. borbonicus have body deep and lateral teeth in jaws with strong molars (Carpenter and Allen, 1989), allows to process a wide range of benthic invertebrate with soft and hard-shelled such as crustaceans, mollusks, and echinoderms (Carpenter, 1996). However, this study shows that L. borbonicus have high food overlap (equals to or more than 0.80) with L. microdon, E. affinis, S. jello and C. chrysophrys based on sharing in small pelagic fish (Clupeidae and Engraulidae). In fact, L. borbonicus shifted to these prey because of their abundance in the Mocha fisheries. Less overlap (≤ 0.14) was between L. nebulosus with other predators and this indicates differences of the food components of L. nebulosus from other species. L. nebulosus mainly feed on mollusks, crustaceans and echinoderms besides small proportion of benthic fish (Mullidae, Lutjanidae) while fish prey (especially pelagic fish) dominated in the food of other predators. The overlap between L. lentjan with many of studied species was close to a considerable overlap (0.60), signals that L. lentjan share some preys with these predators but in deferent percentages. Clupeidae formed small percentage in the food of L. lentjan, but it was main prey for other species. The previous studies on food overlap in other areas reported that the low food overlap between species is due to difference in time and place of dietary resource use (Moore and Moore, 1976; Burke, 1995) in addition to the difference in morphology and body size of species (Darnaude et al., 2001). The information got by this study would be useful as a first step for the transition from single-species management to ecosystem-based management. This information will also help in a better understanding of the dietary interactions among predators and prey. More extensive field and laboratory work are required to get more qualitative and quantitative information about habitat, prey availability, long-term trend in the existence of prey in the diet of predators and predation pressure in order to fully understand the dietary interaction between species and their effects on ecology and production of fisheries. Under the few studies on the Mocha fisheries, this information can provide an introductory framework for further investigation on these fisheries. Acknowledgments I wish to express my gratitude to Dr. Mohammed Kaid Hassan for suggesting this problem and helping through the first stage of fieldwork. Sincere thanks for Dr. Fahmy Alslwy for his assistance during data analysis stage and to Amin Allahabi for his language review. Special thanks to Mr. Smeer and Mr. Mohammed for their facilitation during fieldwork at Mocha’s fishing landing site. The authors thank the Algerian Ministry for Higher education and scientific research who financed this research as part of a thesis grant awarded to N. A. M. Al Kamal. References Al-Zibdah, M., Odat, N., 2007. FisherY status, growth, reproduction, biology and feeding habit of two scombrid fish from the Gulf of Aqaba, Red Sea. Marine Science Station, P.O. Box 195, Aqaba. Jordan. Lebanese Sci. J. 2, 3–20. Alabsi, N., Komatsu, T., 2014. Characterization of fisheries management in Yemen: a case study of a development country’s management regime. Mar. policy. 50, 89–95.

12

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693

Ali, M.K.H., Belluscio, A., Ventura, D., Ardizzone, G., 2016. Feeding ecology of some fish species occurring in artisanal fishery of Socotra Island (Yemen). Mar. Pollution Bull. 105, 613–668. Anderson, G.R.V., Ehrlinch, A.H., Ehrlinch, P.R., Roughgarden, J.D., Russel, B.C., Talbot, F.H., 1981. The community structure of coral reef fishes. Am. Nat. 117, 476–495. Bachok, Z., Mansor, M.I., Noordin, R.M., 2004. Diet composition and food habits of demersal and pelagic marine fishes from Terengganu waters, east coast of Peninsular Malaysia. Naga, WorldFish Center Q 27, 41–47. Baker, R., Sheaves, M., 2005. Redefining the piscivore assemblage of shallow estuarine nursery habitats. Mar. Ecol. Prog. Ser. 291, 197–213. Bakhoum, S.A., 2007. Diet overlap of immigrant narrow–barred spanish mackerel Scomberomorus commerson (Lac., 1802) and the largehead hairtail ribbonfish Trichiurus lepturus (L., 1758) in the Egyptian Mediterranean coast. Animal Biodiversity Conservat. 2, 147–160. Banse, K., 1987. Seasonality of phytoplankton chlorophyll in the central and northern Arabian Sea. Deep-Sea Res. 34, 713–723. Barry, J.P., Ehret, M.J., 1993. Diet, food preference, and algal availability for fishes and crabs on intertidal reef communities in southern California. Environ. Biol. Fish. 37, 82–92. Beyst, B., Cattrijsse, A., Mees, J., 1999. Feeding ecology of juvenile flatfishes of the surf zone of sandy beach. J. Fish Biol. 55, 1172–1186. Blaber, S.J.M., Cyrus, D.P., 1983. The biology of Carangidae (Teleostei) in Natal estuaries. J. Fish Biol. 22, 173–188. Blaber, S.J.M., Milton, D.A., Rawlinson, N.J.F., Sesewa, A., 1993. Predators of tuna baitfish and the effects of baitfishing on the subsistence reef Fisheries of Fiji. In: Blaber, S.J.M., Milton, D.A., Rawlinson, N.J.F. (Eds.), Tuna Baitfish in Fiji and Solomon Islands: Proceedings of a Workshop, Suva, Fiji, 17-18 August 1993, Vol. 52. Australian Centre for International Agricultural Research, pp. 51–61. Blaber, S.J.M., Milton, D.A., Rawlinson, N.J.F., Tiroba, G., Nichols, P.V., 1990. Diets of lagoon fishes of the Solomon Islands: Predators of tuna baitfish and trophic effects of baitfishing on the subsistence fishery. Fish. Res. 8 (3), 263–286. Brewer, D.T., Warburton, K., 1992. Selection of prey from a seagrass / mangrove environment by golden lined whiting, Sillago analis (Whitley). J. FishBiol. 40, 257–271. Brodie, J., Al-Sorimi, M., Turak, E., 1999. Fish and Fisheries of Yemen’s Red Sea. In: DouAbul, A., Rouphael, T.S., Marchant, R. (Eds.), Ecosystems of the Red Sea Coast of Yemen. Hassall and Associates, Australian Marine Science and Technology Ltd (AMSAT) for the United Nations Office for Project Services (UNOPS). pp. 51–72. Burke, J.S., 1995. Role of feeding and prey distribution of summer and southern flounder in selection of estuarine nursery habitats. J. Fish Biol. 47, 355–366. Cabral, H.N., Lopes, M., Loeper, R., 2002. Trophic niche overlap between flatfishes in a nursery area on the Portuguese coast. J. Scientia Marina. 66 (3), 293–300. Carpenter, K.E., 1996. Morphometric pattern and feeding mode in emperor fishes (Lethrinidae, Perciformes). In: Marcus, L.F., et al. (Eds.), Advances in Morphometrics. Plenum Press, New York, pp. 479–487, http://link.springer. com/chapter/10.1007%2F978-1-4757-9083-2_41. Carpenter, K.E., Allen, G.R., 1989. FAO species catalogue. Vol., 9. Emperor fishes and large-eye breams of the world (family Lethrinidae). An annotated and illustrated catalogue. of Lethrinidae species known to date. FAO Fisheries Synopsis. 125 (9), 118. Carpenter, E.K., Krupp, F., Jones, D.A., Zajonz, U., 1997. The Living Marine Resources of Kuwait, Eastern Saudi Arabia, Bahrain, Qatar and the United Arab Emirates. FAO Species Identification Field Guide for Fishery Purposes, Food and Agriculture Organization of the United Nations, Rome, Italy, ISBN: 9251037418, p. 239. Chabanet, P., Durville, P., 2005. Reef fish inventory of juan de nova′ s natural park. West Ind. Ocean J. Mar. Sci. 2, 145–162. Clarke, K.R., Gorley, R.N., 2001. Primer v5: User Manual/ Tutorial, PRIMER-E Ltd., Plymouth Marine Laboratory Prospect Place West Hoe, Plymouth PLI 3DH, United Kingdom. Clarke, K.R., Warwick, R.M., 1994. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. Natural Environmental Research Council, U.K. (144pp.). Coleman, C.F., Koenig, C.C., Huntsman, G.R., Musick, J.A., Eklund, A.M., McGovern, J.C., Chapman, R.W., Sedberry, G.R., Grimes, C.B., 2000. Long-lived reef fishes: the grouper-snapper complex. Fisheries. 25, 14–20. Costa, C., Cataudella, S., 2007. Relationship between shape and trophic ecology of selected species of sparidae of the Caprolace coastal lagoon (Central Tyrrhenian Sea). Environ. Biol. Fish. 78, 115–123. Dalzell, P., 1996. CaTch rates, selectivity and yields of reef fishing. In: Polunin, N.V.C., Roberts, C.M (Eds.), Tropical Reef Fisheries. Chapman and Hall, London, pp. 161–192. Darnaude, A.M., Hamelin-Vivien, M.L., Salen-Picard, C., 2001. Food portioning among flatfish (pisces: Pleuronectiforms) juveniles in mediterranean coastal shallow area. J. Mar. Biol. Ass. U.K 81, 119–127.

De Souza, S.N., Kumar, M.D., Sardesai, S., Sarma, V.V.S.S., Shirodkar, P., 1996. Seasonal variability in oxygen and nutrients in the central and eastern Arabian Sea. Current Sci. 71 (847), https://www.researchgate.net/profile/ Sarma_Vvss/publication/27666819. DouAbul, A., Haddad, A., 1999. The red sea and yemen’s red sea environments. In: DouAbul, A.A-Z., Rouphal, T., Marchant, R. (Eds.), Ecosystems of the Red Sea Coast of Yemen. Hassall and Associates, Australian Marine Science and Technology Ltd (AMSAT) for the United Nations Office for Project Services (UNOPS). pp. 1–16. Dulvy, N.K., Freckleton, R.P., Polunin, N.V.C., 2004. Coral reef cascades and the indirect effects of predator removal by exploitation. Ecol. Lett. 7, 410–416. Durville, P., Chabanet, P., Quod, J.P., 2003. Visual census of the reef fishes in the natural reserve of the glorieuses islands (western Indian ocean). Western Ind. Ocean J. Mar. Sci. 2, 95–104. Edwards, F.J., 1987. Climate and oceanography. In: Edwards, A.J., Head, S.M. (Eds.), Red Sea. Pergamon press, Oxford, pp. 45 – 69. Egretaud, C., 1992. Étude de la biologie générale et plus particulièrement du régime alimentaire de Lethrinus nebulosus du lagon d’Ouvéa. DAA, ENSA Rennes Halieutique. ORSTOM. Sci. Vie: Biol. Mar. 103. Fischer, W., Bianchi, G. (Eds.), 1984. FAO Species identification sheets for fishery purposes. western Indian Ocean; (Fishing Area 51). In: Prepared and Printed with the Support of the Danish International Development Agency (DANIDA). Rome, FAO of the United Nations. Godcharles, M.F., Murphy, M.D., 1986. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (south Florida), king mackerel and Spanish mackerel. U. S. Fish Wildl. Serv. Biol. Rep. 82(11.58).U. S. Army Corps of Engineers, TR EL-82-4.18. Halim, Y., 1969. Plankton of the red sea. Oceanogr. Mar. Biol. Ann. Rev 7, 231–275. Hall, S.J., Raffaelli, D., Basford, D.J., Fryer, M.R., Robertson, R., 1990. The feeding relationships of the larger fish species in a Scottish sea loch. J. Fish Biol. 37, 775–791. Hart, P.J.B., Ison, S., 1991. The influence of prey size and abundance, and individual phenotype on prey choice by the three-spined stickleback, Gasterosteus aculeatus L. . J. Fish Biol. 38, 359–372. Hosseini, S.A., Jamili, S., Valinassab, T., Vosoghi, G., Fatemi, S.M.R., 2009. Feeding and spawning of Sphyraena jello in the North-West of Persian Gulf. J. Fisheries Aquat. Sci. 4, 57–62. Hunt, C., 2003. Economic globalization impacts on Pacific marine resources. Mar. Policy 27, 79–85. Hyslop, E.J., 1980. Stomach content analysis: A review of methods and their application. J. Fish Biol. 17, 411–422. Jennings, S., Greenstreet, S.P.R., Reynolds, J.D., 1999. Structural change in an exploited fish community: a consequence of differential fishing effects on species with contrasting life histories. J. Animal Ecol. 68, 617–627. Jennings, S., Lock, J.M., 1996. Population and ecosystem effects of reef fishing. In: Polunin, N.V.C., Roberts, C.M. (Eds.), Reef Fisheries. Chapman and Hall, London, pp. 193–218. Jeyaseelan, M.J.P., 1998. Manual of Fish Eggs and Larvae from Asian Mangrove Waters. United Nations Educational, Scientific and Cultural Organization, Paris, p. 193. Kulbicki, M., Bozec, Y.M., Labrosse, P., Letourneur, Y., Mou-Tham, G., Wantiez, L., 2005. Diet composition of carnivorous fishes from coral reef lagoons of new Caledonia. Aquat. Living Resour. 18, 231–250. Lasiak, T.A., Mclachlan, A., 1987. Opportunistic utilization of mysid shoals by surf zone teleosts. Mar. Ecol. Prog. Ser. 37, 1–7. Linder, T., 2010. Marine Invertebrates. Zanzibar Field Study, University Bonn. Madhupratap, M., Prasanna, K.S., Bhattathiri, P.M.A., Kumar, M.D., Raghukumar, S., Nair, K.K.C., Ramaiah, N., 1996. Mechanism of the biological response to winter cooling in the northeastern Arabian Sea. Nature. 384, 549–552. Mohanraj, T., Prabhu, K., 2012. Food habits and diet composition of demersal marine fishes from gulf of mannar, southeast coast of india. Advan. Biol. Res. 6 (4), 159–164. Moore, J.W., Moore, I.A., 1976. The basis of food selection in flounders, platichthtys flesus (L), in the Severn estuary. J. Fish Biol. 9, 139–156. Parsons, T.R., 1996. Theimpactof industrial fisheries on the trophic structure of marine ecosystems. In: Polis, G.A., Winnemiller, K.D. (Eds.), Marine Food Webs: Integration of Patterns and Dynamics. Chapman and Hall, New York, pp. 352–357. Pauly, D., 1997. Small-scale fisheries in the tropics: mariginality, marginalization and some implications for fisheries management. In: Pikitch, E.K., Huppert, D.D., Sissenwine, M.P. (Eds.), Global Trends: Fisheries Management, Vol. 20. American Fisheries Society Symposium, Bethesda, pp. 40–49. PERSGA, 2002. Strategic action programme for the Red Sea and Gulf of Aden: Status of the Living Marine Resources in the Red Sea and Gulf of Aden and Their Management. Reegional Organization for the Conservation of the Environment of the Red Sea and Gulf of Aden (PERSGA), First Printing May 2002.148p.. Platell, M.E., Potter, I.C., 2001. Partitioning of food resource amongst 18 abundant benthic carnivorous fish species in marine waters on the lower coast of Australia. J. Exp. Mar. Biol. Ecol. 261, 31–34.

N.A.M. Al Kamel and M.H. Kara / Regional Studies in Marine Science 29 (2019) 100693 Poore, G.C.B., 2004. Marine Decapod Crustacea of Southern Australia A Guide to Identification. (617pp). Quinn, G.P., Keogh, M.J., 2002. Experimental Design and Data Analysis for Biologist. Cambridge University Press, Cambridge, pp. 426–493. Roberts, C.M., 1995. Effects of fishing on the ecosystem structure of coral reefs. Conserv. Biol. 9, 988–995. Sabrah, M.M., El-Ganainy, A.A., 2009. Observation on biological traits of striped goatfish (Upeneus vittatus) and Freckled Goatfish (Upeneus tragula) from the Gulf of Suez, Egypt. World J. fish Mar. Sci. 1 (2), 121–128. Sadovy, Y., 2001. The threat of fishing to highly fecund fishes. J. Fish Biol. 59, 90–108. Salini, J.P., Blaber, S.J.M., Brewer, D.T., 1994. Diets of trawled predatory fish of the gulf of Carpentaria with, Australia, particular reference to predation on prawns. Aust. J. Mar. Freshwat. Res. 45 (3), 397–411. Schott, F., Swallow, J.C., Fieux, M., 1990. The somalia current at the equator: annual cycle of currents and transports in the upper 1000 m and connection to neighboring latitudes. Deep-Sea Res. 37, 1825–1848. Stergiou, K.I., Fourtouni, H., 1991. Food habits, ontogenetic diet shift and selectivity in Zeus faber Linnaeus 1758. J. Fish Biol. 39, 589–603. Takeuche, N., Toshifumi, S., Yoichi, S., Hiroaki, H., 2007. Diets of 45 species from 17 families at Kuchierabu-jima Island. J. Grad. Sch. Biosp. Sci. Hiroshima Univ. 46, 5–13. Tesfamichael, D., 2016. An exploration of ecosystem-based approaches for the management ofred sea Fisheries. In: Tesfamichael, D., Pauly, D. (Eds.), The Red Sea Ecosystem and Fisheries. Coral Reefs of the World 7. Springer Science+Business Media Dordrecht, pp. 111–134. http://dx.doi.org/10.1007/ 978-94-017-7435-2_1t, http://www.springer.com/series/7539.

13

Tesfamichael, D., Pitcher, T.J., Pauly, D., 2014. Assessing changes in fisheries using fishers knowledge to generate long time series of catch rates: a case study from the red sea. Ecol. Soc. 19 (1), 18. http://dx.doi.org/10.5751/ES-06151190118. Tesfamichael, D., Rossing, P., Saeed, H., 2016. Yemen. In: Tesfamichael, D., Pauly, D. (Eds.), The Red Sea Ecosystem and Fisheries. Coral Reefs of the World 7. Springer Science+Business Media Dordrecht, pp. 65–77. http:// dx.doi.org/10.1007/978-94-017-7435-2_1t, http://www.springer.com/series/ 7539. Tharwat, A.A., Al-Gaber, A., 2006. FisherY Traps (Gargours) in Saudi Territorial Waters of the Arabian Gulf. JKAU: Mar. Sci. 17, 13–31. Toor, H.S., 1964. Biology and fishery of the pig-face bream, Lethrinus lentjan (Lacepède). I. Food and feeding habits. Indian J. Fish. 11 (2), 559–580. Tsehaye, I., 2007. Monitoring Fisheries in Data-Limited Situations: A Case Study of the Artisanal Reef Fisheries of Eritrea (Ph.D. thesis). Wageningen University, the Netherlands, p. 183. Walker, M.H., 1978. Food and feeding habits of Lethrinus chrysostomus Richardson (Pisces: Perciformes) and other Lethrinidae on the Great Barrier Reef. Aust. J. Mar. Freshwater. Res. 29 (5), 623–630. Wallace, H., 1981. An assessment of diet overlaps indices. Trans. Am. Fish. Soc 110, 72–76. Windell, J.T., Bowen, S.H., 1978. Method for study of fish diets based on analysis of stomach contents. In: In Methods for the Assessment of Fish Production in Fresh Water. Third (T. Bagenal, Ed), Pp., 219-226. Oxford Blackwell Science. Public, p. 365. Wolfgag, S., 1986. Marine fauna and flora Bermuda. A systematic guide to the identification of marine organisms (742 pp). Zaret, T.M., Rand, A.S., 1971. Competition in tropical season fishes: Support for the competitive exclusion principle. Ecology. 52, 336–342.