Introduction

Different types of abnormalities including those of the color were documented on several species of fishes since the works of Dawson (1964; 1966; 1971) (Macieira et al., 2006; Simon et al., 2009). Malpigmentation in fishes generally occurs as either a deficiency (albinism or hypomelanosis) or an excess (melanism or hypermelanosis) of pigmentation (Simon et al., 2009; Jawad et al., 2013). Xanthism or xanthochroism is a certain form of hypomelanism, where the bright yellow or orange body coloration became prevailing (Carson, 2011; Lewand et al., 2013). Economically, any changes in the normal coloration of the fish will have a negative marketing impacts impact as it can discourage the customer from buying and on the survival of the fish in the environment (Heemstra and Randall, 1993). Malpigmentation in teleosts has been widely studied in Pleuronectiform fishes in relation to developing asymmetry (Matsumoto and Seikai, 1992; Venizelos and Benetti, 1999; Barton, 2010), but it has been also noticed in other fish groups in the wild but to a lesser extent (Deynat, 2003; Feitoza et al., 2003; Brito and Caramasch, 2005; Sampaio et al., 2006; Jawad et al., 2013).

The whitebarred rubberlip Plectorhinchus playfairi is a marine species found living in the reef’s area at depth range from surface down to 80 m (Smith and McKay, 1986). It distributed in the western Indian Ocean from the Red Sea in the north and southward to eastern coasts of South Africa and Madagascar including Saudi Arabia (Randall, 1995; Jawad and Ibrahim, 2014). This species is characterised in having body with black color in general, with white vertical bars running across (Lieske and Myers, 1994).

The epaulet grouper Epinephelus stoliczkae is a marine species inhabits coral reef’s areas at depth range 5-50 m. This species is distinguished in its coloration among the other species of the genus Epinephelus. The head and body are yellow to grey, with dark orange spots except ventrally and posteriorly. Presence of dark grey bars below the posterior part of the dorsal fin. The distribution of this species is confined to the Red Sea, north of the Arabian Sea and the Sea of Oman (Craig et al., 2011).

Jawad and Al-Mamry (2009), Jawad and AL-Kharusi (2013), Jawad et al. (2013) and Jawad and Ibrahim (2014) were the only works have been performed on the color aberration in fishes from the Arabian Gulf and the Sea of Oman areas. No previous studies on ambicoloration of P. playfairi have been done in these areas before. For E. stoliczkae, this is the 2^nd report on color aberration. Jawad and Al-Kharusi (2013) reported on color anomalies in this species from Sea of Oman. Therefore, the result of the present study is considered the first record of color aberration in P. playfairi and the 2^nd for E. stoliczkae from these areas. The purpose of this study is to describe the occurrence ambicoloration in 2 fish species collected from the Arabian Gulf waters of Saudi Arabia.

1 Material and Methods

Two specimens of the family Haemulidae, 1 specimen of Plectorhinchus playfairi (TL 346), 1 specimen of Plectorhinchus sordidus (TL 357 mm), and 3 specimens of Epinephelus stoliczkae (TL 424-429 mm) were shown aberrant coloration. Species of the family Haemulidae were captured in the period of 26^th February 2013 to 21^st September 2016 in the waters of Jubail City Saudi Arabia. The specimens were collected by local fishermen using drifting gill net. Specimens of E. stoliczkae were obtained from the frozen fish market in Jubail City, Saudi Arabia. The origin of these specimens was traced back to several localities in the neighboring Sultanate of Oman. Normal specimens with normal coloration were obtained from the same fishing lot at the same fishing locality to make a comparison. Body and fins were examined carefully for external parasites, malformations, amputations and any other morphological anomalies. The specimens were deposited in the fish collection of the Fish Welfare Branch, Jubail, Saudi Arabia. Once in the laboratory, measurements were recorded to the nearest millimetre.

2 Results

Ambicoloration cases were observed in the two species of the two families studied. The description of the aberrant coloration distribution in each species studied is given below based on the case of color abnormality.

Family: Epinephelidae

Epinephelus stoliczkae

Colour of normal specimen (Figure 1):

Body and head greyish yellow, with dark orange-red spots distributed in the anterior half of the body and on its ventral side. Presence of 3 dark bars, 2 below the soft part of the dorsal fin and 1 at the base of the caudal fin. Pectoral fin dark sometimes with dark blotch at its base. The remaining fins are with dark yellowish grey color.

Colour of abnormal specimens

Specimen no.1 (TL, 424 mm) (Figure 2):

The majority of the normal coloration was disappeared and instead a bog pale patch covering the body except for a triangular area of the normal body coloration covering the head and a narrow strip behind the head. The pale patch extended posteriorly to the base of the caudal fin. The dark spots on body were slightly affected with color aberration. The color of the 3 dark bars was faded.

Specimen no.2 (TL 426 mm) (Figures 3A; Figure 4A):

The left side of this specimen was slightly affected with the color aberration. The following areas were shown to have pale patches: anterior to posterior, the ventral side of the operculum, pectoral fin, areas under the spinous and soft parts of the dorsal fin and caudal peduncle. The color on the right side of this specimen is more affected than the left side. A continuous pale patch extending from posterior of the head to the base of the caudal fin.

Specimen no.3 (TL 427 mm) (Figures 3B; Figure 4B):

The normal coloration on the left side of fish body was severely deformed. A triangular patch of the normal body color covering the whole head and a moderate stripe behind it. The ventral side of the head, pectoral fin and the base of the caudal fin were shown to be affected (Figure 3B). The right side of the fish body showed to have two rounded patches, one extended from the posterior edge of the eye to the mid of the spinous part of the dorsal fin. This patch extend ventral to cover the pectoral fin. The other pale patch extended from the posterior tip of the pectoral fin to the posterior tip of the anal fin.

Family: Haemulidae

Plectorhinchus sordidus

Colour of normal specimen (Figure 5):

Body grey in color, with a bronze shading. Dark brown operculum membrane. All fins are dark.

Colour of abnormal specimens

Specimen no 1 (TL: 357 mm) (Figure 6; Figure 7; Figure 8):

The main part of the left side of the fish body is covered with large pale patch and the normal coloration was aberrated and only five main patches were left. They were distributed from the anterior to the posterior as follows: one elongated patches traversing diagonally dorsal anteriorly from the nape to the just behind the corner of the mouth, a broad patch located below the spinous part of the dorsal fin and beneath the pectoral fin. It extended ventrally to reach the dorsal edge of the ventral fin, a nearly rectangular patch lie at the base of the junction of the spinous and the soft parts of the dorsal fin. Ventrally it extended to the lateral line, a nearly rectangular patch situated below the soft part of the dorsal fin and extended posteriorly to reach the posterior edge of the dorsal fin. It extended ventrally to reach the lateral line and small rectangular patch located dorsal to the base of the anal fin and traverse posterior ventrally on the surface of the anal fin. Few other small patches of the normal coloration were observed on the dorsal side of the head, below the anterior edge of the dorsal fin, below the operculum and at the base of the caudal fin. The caudal fin showed to be color aberrated (Figure 6). The right side of the fish was less aberrated than the left side. Here, big patch in the shape of backward reversed “L-shaped” was located from the nape to the anterior edge of the dorsa fin. It extended ventrally to reach the area from the operculum to the anterior end of the anal fin. Pale narrow patches were found along the posterior ventral edge of preoperculum and operculum. Few small patches of the normal coloration were found on the caudal peduncle. The caudal fin showed to be color aberrated (Figure 7). The ventral side of the fish body showed small dark patches on the gular area and under the pectoral fins (Figure 8).

Plectorhinchus playfairi

Colour of normal specimen (Figure 9):

The color of the body of this species is distinguished in having the dorsal side black and white ventral side. Presence of 4 white vertical bars, 1 across the operculum and 3 extending below the spinous part of the dorsal fin. All fins were black.

Colour of abnormal specimen (TL 346 mm) (Figure 10):

The colour of this specimen was not heavily aberrated. The areas under the operculum, the base of the pectoral fin and the base of the caudal peduncle were shown to have pale patches. The 1^st white bar appeared disturbed with a pale patch.

3 Discussion

The present report is the first record of coloration anomalies in E. stoliczkae, P. playfairi and P. sordidus. According to Craig et al. (2011), E. stoliczkae is not reported from the Arabian Gulf area. As in the other Gulf States, fish commodities imported from abroad and offered for sale in the local fish market. In the case of E. stoliczkae, it is usually imported from Sultanate of Oman.

The pattern of the color aberration case reported for E. stoliczkae by Jawad and Al-Kharusi (2013) from Oman differs completely from the present cases. The specimens examined in this study showed a severe case of color aberration due to the large are affected. The color of the unaffected areas was less visible, while in the case of Jawad and Al-Kharusi (2013) the unaffected areas kept their normal grade of coloration. Unlike the case of Jawad and Al-Kharusi (2013), the pale patch that covered the body of the fish in the present study had no patch of normal coloration. Variation in color aberration between different sites of the fish body might be due to the causes given by Roulin and Ducrest (2011). They found that controlling the genes of the melanocortin system or of their products will have significant effects on a set of characters. Slominski et al. (2000), found that the level of activity of the different melanocortins is correlated across tissues. Other studies indicated that with the aid of neuroendocrine communication, the activity of the melanocortin system can be locally regulated and coordinated (Slominski and Wortsman, 2000) and such manipulation could vary between tissues of the fish body (Hoglund et al., 2000).

Ambicoloration is frequently accompanied by some morphological variation (Díaz de Astarloa, 1995; 1998; Jawad, 2014). No noticeable variation on morphological or meristic characters was found for the ambicolored epinephelid or haemulids species studied.

In fishes, aberration in normal coloration can happened due to several reasons and they are depend on the type of pigmentation disorder. Studies showed that such abnormalities in the color might be as results of wounds or bites (Moe, 1963; Colman, 1972); might have genetic bases (Hernandez and Sinovcic, 1987); might be due to local tissue environment (Seikai, 1992; Seikai and Matsumoto, 1994); might related to diet deficiency (Kanazawa, 1993); increasing water temperature during the larval development might has direct effect on development of skin pigmentation (Aritaki and Seikai, 2004), and disorder in the level of the thyroid hormone might be behind this abnormality (Okada, 2005). Other factor such as the cellular interaction might also contribute to such aberration. The cellular interaction interferes with the control of the pigment cell arrangements on the fish body, which in turn cause malpigmentation in perciform fishes (Lueken et al., 1973). Diseases such as scuticociliatosis and other ciliatosis are believed the cause of the aberration in sea bass for example (FAO, 2005-2012). In Epinephelus coioides, it found that the parasitic infestations by Cryptobia sp, Scyphidia sp. Vorticella sp. Dactylogyrus sp. Neobenedenia girellae, and Gnathia sp. Can cause loss of pigments from the skin (FAO, 2010-2012). Deficiencies in vitamins like C and E could bring color aberration due to loss (Lovell, 1973). In addition, fat level discrepancies in the food content could also lead to loss of pigments in Chinook salmon (FAO, 1980). All the above causes mentioned above could be behind the loss of pigments cases described in the present study. Clearly, a thorough investigation is required to define the cause of depigmentation perceived here, but the present records are nevertheless significant owing to the rarity of the phenomenon in wild populations.

Authors’ contributions

Both authors have contributed equally toward the publication of this paper.

Acknowledgments

We would like to thank the Ministry of Agriculture, Fish Welfare Branch, Jubail Province, Saudi Arabia for giving us the opportunity to examine and study the deformed fish specimens. Our thanks are also due to Sergey Bogorodsky of Station of Naturalists, Omsk, Russia and Ronald Fricke of Staatliches Museum für Naturkunde, Rosenstein, Germany, for identification of the species.

References

Aritaki M., and Seikai T., 2004, Temperature effects on early development and occurrence of metamorphosis-related morphological abnormalities in hatchery-reared brown sole Pseudopleuronectes herzensteini, Aquaculture, 240: 517-530

https://doi.org/10.1016/j.aquaculture.2004.06.033

Barton D., 2010, Flatfish (Pleuronectiformes) chromatic biology, Review in Fish Biology and Fisheries, 20: 31-46

https://doi.org/10.1007/s11160-009-9119-0

Brito M.F.G., and Caramaschi E.P., 2005, An albino armored catfish Schizolecis guntheri (Siluriformes: Loricariidae) from an Atlantic forest coastal basin, Neotropical Ichthyology, 3: 123-125

https://doi.org/10.1590/S1679-62252005000100009

Carson E.W., 2011, Low but stable frequency of xanthic phenotypes in a population of the twoline pupfish, Cyprinodon bifasciatus, American Midland Naturalist, 166: 462-466

https://doi.org/10.1674/0003-0031-166.2.462

Colman J.A., 1972, Abnormal pigmentation in the sand flounder, New Zealand Journal of Marine and Freshwater Research, 6: 208-213

https://doi.org/10.1080/00288330.1977.9515419

Craig M.T., Sadovy de Mitcheson Y.J., and Heemstra P.C., 2011, Groupers of the world, Published by NISC, Grahamstown, South Africa, p.402

Dawson C.E., 1964, A bibliography of anomalies of fishes, Gulf Research Reports, 1: 308–399

https://doi.org/10.18785/grr.0106.01

Dawson C.E., 1966, A bibliography of anomalies of fishes, Gulf Research Reports, 2 (Supplement): 169–176

https://doi.org/10.18785/grr.0202.03

Dawson C.E., 1967, Three new records of partial albinism in American Heterosomata, Transaction of the American Fisheries Society, 96: 400-404

https://doi.org/10.1577/1548-8659(1967)96[400:TNROPA]2.0.CO;2

Deynat P.P., 2003, Albinisme partiel chez le pailona commum, Centroscymnus coelolepis (Elasmobranchii, Somniosidae), Cybium, 27: 233–236

Díaz de Astarloa J.M., 1998, An ambicolorate flounder Paralichthys isosceles (Pleuronectiformes: Paralichthyidae), collected off Península Valdez (Argentina), Cybium, 22: 187-191

Díaz de Astarloa J.M., 1995, Ambicolouration in two flounders, Paralichthys patagonicus and Xystreuris rasile, Journal of Fish Biology, 47: 168-170

https://doi.org/10.1111/j.1095-8649.1995.tb01883.x

FAO, 2005-2012, Cultured Aquatic Species Information Programme, Dicentrarchus labrax. Cultured Aquatic Species Information Programme, Text by Bagni, M. In: FAO Fisheries and Aquaculture Department, Rome

FAO, 2010-2012, Cultured Aquatic Species Information Programme. Epinephelus coioides, Cultured Aquatic Species Information Programme, Text by Shams, A.J. In: FAO Fisheries and Aquaculture Department, Rome

Feitoza B.M., Rosa R.S., and Rocha L.A., 2005, Ecology and zoogeography of deep-reef fishes in northeastern Brazil, Bulletin of Marine Science, 76: 725-742

Heemstra P.C., and Randall J.E. (eds.), 1993, Groupers of the world (Family Serranidae, subfamily Epinephelinae): an annotated and illustrated catalogue of the grouper, rockcod, hind, coral grouper, and lyretail species known to date, FAO fisheries synopsis no. 125: 1-124, Food and Agriculture Organization of the United Nations, Rome

Hernndez V.A., and Sinovcic G., 1987, A note on a partial albino specimen of the species Liza (Liza) ramada (Risso, 1826) caught from the middle Adriatic, Institut za oceanografiju i ribarstvo, 68: 1-4

Hoglund E., Balm P.H.M., and Winberg S., 2000, Skin darkening, a potential social signal in subordinate arctic charr (Salvelinus alpinus): the regulatory role of brain monoamines and pro-opiomelanocortin-derived peptides, Journal of Experimental Biology, 203: 1711–1721

Jawad L.A., and AL-Kharusi L.H., 2013, January, A reported case of abnormal pigmentation in the epaulet grouper Epinephelus stoliczkae (Day, 1875) collected from the Sea of Oman, Anals du Biologia, 35: 41

https://doi.org/10.6018/analesbio.0.35.6

Jawad L.A., and AL-Mamry J., 2009, First record of Antennarius coccineus from the Gulf of Oman and second record of Antennarius indicus from the Arabian Sea coast of Oman, Marine Biodiversity Records, 2

https://doi.org/10.1017/S1755267209990923

Jawad L.A.J., AL-Shogebai S., and AL-Mamry J.M., 2013, A reported case of malpigmentation in the spangled emperor Lethrinus nebulosus (Osteichthyes: Lethrinidae) collected from the Arabian Sea coasts of Oman, Thalassia Salentina, 35: 29-36

Jawad L.A., and Ibrahim M., 2014, Confirmed record of whitebarred rubberlip, Plectorhinchus playfairi (Pellegrin, 1914) (Pisces: Haemulidae) from Jubail, Saudi Arabia, Arabian Gulf. International Journal of Marine Science, 4: 194-196

Kanazawa A., 1993, Nutritional mechanisms involved in the occurrence of abnormal pigmentation in hatchery- reared flatfish, Journal of the World Aquaculture Society, 24: 162-166

https://doi.org/10.1111/j.1749-7345.1993.tb00005.x

Lewand K.O., Hyde J.R., Buonaccorsi V.P., and Lea R.N., 2013, Orange coloration in a black-and-yellow rockfish (Sebastes chrysomelas) from central California, California Fish and Game, 99: 237-239

Lieske E., and Myers R., 1994, Collins Pocket Guide, Coral reef fishes, Indo-Pacific & Caribbean including the Red Sea, Haper Collins Publishers, p.400

Lovell R.T., 1973, Essentiality of vitamin C in feeds for intensively fed caged catfish, Journal of Nutrition, 103: 134-138

Lueken W., Schmidt E.R., and Lepper K., 1973, Regulation of the pigment cell arrangements in species and interspecies hybrids of Xiphophorus (Pisces, Poeciliidae) by cellular interactions on the fish body, In: Genetics and Mutagenesis of Fish, (J. H. Schröder ed.), 139-160, Springer-Verlag Berlin-Heidelberg-New York

https://doi.org/10.1007/978-3-642-65700-9_14

Macieira R.M., Joyeux J.C., and Chagas L.P., 2006, Ambicoloration and morphological aberration in the sole Achirus declivis (Pleuronectiformes: Achiridae) and two other cases of color abnormalities in achirid soles from southeastern Brazil, Neotropical Ichthyology, 4: 287–290

https://doi.org/10.1590/S1679-62252006000200016

Moe M., 1963, Partial albinism in a xanthic specimen of Epinephelus morio (Valenciennes) from the Gulf of Mexico, Copeia, 3: 703

https://doi.org/10.2307/1440977

Okada N., 2005, Development of tissues involved in eye migration and role of thyroid hormone in metamorphosing Japanese flounder (Paralichthys olivaceus). Scientific Report of the Hokkaido Fish Experiment Station, 68: 1-43

Randall J.E., 1995, Coastal fishes of Oman. University of Hawaii Press, Honolulu, Hawaii, p.439

Roulin A., and Ducrest A.L., 2013, Genetics of coloration in birds. Cell Developmental Biology, 24: 594–608

https://doi.org/10.1016/j.semcdb.2013.05.005

PMid:23665152

Sampaio L., and Bianchini A., 2002, Salinity effects on osmoregulation and growth of the euryhaline flounder Paralichthys orbignyanus, Journal of Experimental Marine Biology and Ecology, 269: 187-196

https://doi.org/10.1016/S0022-0981(01)00395-1

Seikai T., and Matsmoto M., 1994, Mechanism of pseudoalbinism in flatfish: an association between pigment cell and skin differentiation, Journal of the World Aquaculture Society, 25: 78-85

https://doi.org/10.1111/j.1749-7345.1994.tb00807.x

Seikai T., 1992, Process of pigment cell differentiation in skin on the left and right sides of the Japanese flounder, Paralichthys olivaceus, during metamorphosis, Japanese Journal of Ichthyology, 39: 85-92

Seikai T., Hirose E., Matsumoto J., 1993, Dual appearances of pigment cells from in vitro cultured embryonic cells of Japanese flounder: an implication for a differentiation–associated clock, Pigment Cell Research, 6: 423-431

https://doi.org/10.1111/j.1600-0749.1993.tb00625.x

PMid:7511808

Sion T., Joyeux J.C., and Machieira R.M., 2009, First record of partial melanism in the coney Cephalopholis fulva (Perciformes: Epinephelidae), Brazilian Journal of Oceanography, 57: 145-147

https://doi.org/10.1590/S1679-87592009000200007

Slominski A., and Wortsman J., 2000, Neuroendocrinology of the skin. Endocrine Review, 21: 457–487

https://doi.org/10.1210/edrv.21.5.0410

PMid:11041445

Slominski A., Tobin D.J., Shibahara S., and Wortsman J., 2004., Melanin pigmentation in mammalian skin and its hormonal regulation, Physiological Review, 84: 1155–1228

https://doi.org/10.1152/physrev.00044.2003

PMid:15383650

Smith M.M., and McKay R.J., 1986, Haemulidae, p. 564-571, In M.M. Smith and P.C. Heemstra (eds.) Smiths' sea fishes, Springer-Verlag, Berlin

https://doi.org/10.1007/978-3-642-82858-4

Venizelos A., and Benetti D.D., 1999, Pigment abnormalities in flatfish, Aquaculture, 176: 181–188

https://doi.org/10.1016/S0044-8486(99)00060-5