FEEDING HABITS OF THE SUEZ CANAL MIGRANT SQUIRRELFISH, SARGOCENTRON RUBRUM,IN THE MEDITERRANEAN SEA

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1 ISRAEL JOURNAL or ZOOLOGY, Vol. 3, 983, pp FEEDING HABITS OF THE SUEZ CANAL MIGRANT SQUIRRELFISH, SARGOCENTRON RUBRUM,IN THE MEDITERRANEAN SEA D. GOLANI AND A. BEN-TuVIA Department ofzoology, The Hebrew University ofjerusalem, Jerusalem 9904 Israel AND B. GALIL Department ofzoology, Tel Aviv University, Tel Aviv Israel ABSTRACT The squirrelfish, Sargocentron rubrum (Forsskat, 75), is a successful Suez Canal immigrant common along the Mediterranean coast of Israel and caught occasionally in small quantities in commercial catch by trammel net and by hook-and-iine. Monthly samples of stomach contents of this fish caught off 'Akko (Acre), israel, from October 979 to October 980 were examined. Decapoda constituted the bulk of the diet. the remainder being Polychaeta, lsopoda, Mollusca and fishes. S. rubrum feeds intensively in summer and lightly in winter. Seasonal predominance of each taxon in the diet was measured by an alimentary coefficient calculated as a product of the frequency and weight percentages. Brachyura constituted 7.8% in summer, 94.7% in fall and winter; Anomura constituted 8.4% in spring. Pisidia longimana. Portunus hastatus. Xantho spp. and Pilumnus.hirtellus were the most commonly-found prey. No preference for feeding on Suez Canal invflrtebrate immigrants of Red Sea origin was observed. It is concluded that S. rubrum inhabits rocky bottom, at depths of 0-40 m and feeds at night. INTRODUCTION The squirrelfish Sargocentron rubrum (Forsskal, 775)' of the family Holocentridae is one of the early Indo-Pacific Suez Canal immigrants to the eastern Mediterranean. It was recorded for the first time in the Mediterranean Sea from the coast of Israel by Haas and Steinitz (I947) and later from Greece (Laskaridis, 948), Turkey (Kosswig, 950), Libya (Stirn, 970), and Lebanon (Mouneimne, 977) (for summary of records see Ben-Tuvia, 966, 978). S. rubrum in the eastern Mediterranean inhabits rocky grounds at depths of O~40 m (Riedl, 966; Golani, 98). It is caught in some numbers by trammel net and hook-and-iine and, rarely, by trawl. In general, holocentrids are known to be nocturnal and prey chiefly on decapods (Woods & Sonoda, 973; Gladfelter & Johnson, 983). A preliminary examination of I This holocentrid was usually classified in the genus Holocentrus in the older Uterature and in Adioryx in more recent papers. Matsuura and Shimizu ( 98}, however, have shown that the older generic name Sargocentron Fowler must replace Adioryx. Received 3 October 983 and in revised form 7 February 984

2 Vol. 3, 983 FOOD HABITS OF SQUIRRELFISH 95 some stomach contents of S. rubrum from the Mediterranean coast of Israel (Ben Tuvia, 966) also indicated a preference for decapods. The objectives of the present study were to investigate the feeding habits of S. rubrum in its new Mediterranean Sea habitat and to compare its feeding with that of holocentrids from other regions. This was part of a study of the biology of S. rubrum that included age determination, growth and reproduction (Golani, 98). MATERIAL AND METHODS A sample of 3-50 specimens, caught by trammel net, was obtained each month (except April) during the period October 979 to October 980 at the fishing harbour of 'Akko (Acre), Israel. Stomach contents were removed and sorted. Food items were identified as precisely as possible and counted. Total weight of each food item was recorded for each sample and summarized monthly. Most crustaceans and molluscs were well preserved and therefore easily identified. In the case of damaged specimens of crustaceans only carapaces were counted, with the exception of alpheids where chela were counted as evidence. Unidentified food material was weighed and recorded but not included in the calculations of the indices and coefficients. Stomach contents of monthly samples are listed in Table I. Data were analysed by a method similar to that of Hureau (I 970), Vivien (973) and Vivien and Peyrot Clausade (974). The following indices and coefficients were used: N number of fish per sample; Nf - number of fish with stomach contents; n - number of fish with the particular food item (taxon); f - occurrence index = n/nf; Uf - weight of unidentified food material; No - number of organisms in stomach content of all samples in a season; Wf - weight of organism in stomach content of all samples in a season; Os average number of organisms per stomach with content; Ws average weight of organisms pet stomach with content; Cn - percentage of number of organisms of particular taxon in total number of organisms found in all samples in a season; Cw percentage of weight of organisms of particular taxon in total weight of organisms found in all samples in a season; Q alimentary coefficient Cw X Cn. The coefficient Q measures the importance of each taxon relative to the other components of the diet. The following scale of importance was arbitrarily determined: Q'" 0 =: incidental prey 0 '" Q'" 00 =: occasional prey 00 '" Q'" 000 =: secondary prey 000 '" Q primary prey. RESULTS Sargocentron rubrum feeds heavily in summer and lightly in winter. In the colder season, October to May, the percentage of fish with food in the stomach was rather low, 0-78%, compared to 80-95% in the warmer months, June-September. Seasonal differences in feeding intensity are seen more clearly when comparing the

3 96 D. GOLANI ET AL. Isr. J. Zool. TABLE I Number of food organisms in stomach contents of monthly sample of Sargocentron rubrum 30.X.79 9.XI XII N=0 N 9 N= 3 N=0 Nt= Nt= Nt= 7 Nt= 9 Polychaeta 8 Crustacea Isopoda Decapoda Macrura Penaeus sp. Trachypenaeus curvirostris ' Sicyonia cannata Athanas nitescens Alpheus dentipes Alpheui edwardsi Alpheus sp. Synalpheus ganbarelloides Synalpheus hululensis' Syna/pheus sp. Processa nouveli noulleli Processidae Pontophilus tasciatus Upogebia pusilla Upogebia delatura Upogebia sp. Shrimp larvae Anorimra Pagunidae Diogenes pugilator Galathea sp. Pisidia longimana 3 Brachyura Ebalia sp. Myratugax' Leucosia signata' Leucosidae Ixa monodi' Ilia nucleus Macropipus sp. Charybdis longicollis' Charybdis sp. Portunus hastatus 4 Portunus pelagicus' Portunus sp. Xantho poressa Xantho granulicarpus Red Sea migrant.

4 Vol. 3, 983 FOOD HABITS OF SQUIRRELFISH 97.II.80 4.l.80 7.V V VI VIII.80 6.X.80 6X80 N""34 N"" N =3 N 39 N=50 N N 0 N=5 Nf""9 Nf=5 Nf= 5 Nf=37 Nf=44 Nf=7 Nf= 6 Nf=

5 98 D. GOLANI ET AL. lsr. J. Zool. TABLE I (Cont.) 30.x.79 9.xl xIl.79 4.l.80 N=0 N=9 N=3 N= 0 Nf= Nf= Nf= 7 Nf=9 Xantho sp. 4 Pilumnus hirtellus Parthenope sp. Maja verrucosa Pisa muscosa Pisa nodipes Acanthonyx lunuliltus Mollusca Polyplacophora Acanthochitona communis Callochchiton lea vis Chiton olivaceus Chiton corallinus Chiton sp. Gastropoda Emarginula sicula Haliotis (Sulculus) tuberculilta lilmellosa Turbona (Acinu{us) cimex Bittium reticuliltum Cerithium scabridum Lamellilria perspicua Collfmbella rustica Anachis (Zafra) selasphora Na~sarius (Hima) incrassatus Chrysallida maiae l Gastropod unidentified Bivalvia Lima (Mantellum) hians 4 Lima (Mantellum) inflata Fishes Angilliformes Blenniidae Gobiidae Unidentified.. I Red Sea migrant.

6 Vol. 3, 983 FOOD HABITS OF SQUIRRELFISH 99./l V Vl V/l V/[.80 6.X.80 6.x.80 N=34 N= N=3 N 39 N 50 N= N=0 N=5 Nf= 9 Nf= 5 Nf=5 Nf=37 Nf=44 Nf= 7 Nf=6 Nf=

7 00 D. GOLAN I ET AL. Isr. J. Zool. if) I- 8 z W I- 6 t I 4 ~ 0 I- if) U- C 0 l- I Q 08 w ~ w 06 l'l.. a:: w 04.. > ~.. a:: w 4 >.. N 0 M A M A S Fig.!. Average weight offood contents (--) and average number of food organisms (...) per stomach with content. numbers of organisms and weight per fish stomach: organisms and g per filled stomach in June-September as compared to organisms and g per filled stomach in October-May (Fig. ). Table I gives a list of organisms and their occurrence in each sample. The following taxa were present: Poly chaeta, Crustacea (lsopoda, Macrura, Anomura and Brachyura), Mollusca and Pisces. Decapod.crustaceans were a major diet component throughout the year (Table II). From June to September brachyuran crustaceans comprised 77.9% of the alimentary coefficient (Q); all the other invertebrate groups were of secondary or occasional importance, while the presence of fish in the diet was incidental The importance of brachyurans in the diet was even more pronounced in the period October-January, amounting to 84.7%. In February-May the principal components were anomuran decapods, mainly Pisidia iongimana (84.8%). Among polychaetes, Eunicidae and Aphroditidae showed the highest frequency of occurrence, especially in the warmer months (Ben-Eliahu et al, 983). A similar trend of seasonal occurrence was observed in isopods and molluscs. Only two species of decapod, Pisidia iongimana and Piiumnus hirtellus, appeared in the stomach contents throughout the year in sufficient number to suggest an annual distribution in their habitat. Monthly average numbers of these decapods in the fish stomachs (including empty stomachs) show that preying on Pisidia iongimana is year-round, peaking in March and July, while preying on Piiumnus hirtellus peaks distinctly (4.57 crabs per stomach) in August. Based on available information concerning the ecological distribution of the food organisms along the coast of Israel, it is evident that S. rubrum feeds chiefly on rocky substrate, partially covered by seaweeds, and to a much lesser extent on soft bottom (Table III). Among the less frequent food items Myra fugax and Charybdis iongicollis

8 -< f. "" N... '" 00 "" TABLE II Seasonal variation in the diet of S. rubrnm according to taxonomic groups' October-January February-May June-September N =94 No = 78 N 87 No 60 N '" 0 No'" 076 o Nf=48 Wf =. 758 Nf=48 Wf 3.46 Nf= 98 Wf = Os =3.708 Os'" 3.65 Os =.000 "::r: ) Uf=5.9 Ws '" Uf=.00 Ws 0.70 Uf=.753 Ws = 0.80 I::tl ::; CIl n f Cn Cw Q n f Cn Cw Q n f Cn Cw Q o "! Polychaeta CIl g Isopoda ~ Decapoda ~ Macrura I'"' "! Anomura Cii Brachyura ::r: Mollusca Fish I For explanation of indices see text..." N o...

9 ~.. 0 D. GOLANI ET AL. I sr. J. Zool. TABLE III Depth and habitat of the most common decapods found in S. rubrum stomachs l Species Depth (m) Habitat Alpheus dentipes 8-7 Rocks and algae Processa nouveli nouveli 8-35 Soft bottom Pisidia longimana Shallow waters Portunus hastatus 8-33 Rocks Xantho granulicarpus 7-46 Rocks Pillumnus hirtellus 5 Rocks and algae?isa nodipes 8-75 Algae Acanthonyx lunulatus Rocks and algae According to Holthuis & Gottlieb, 958; ZariqueY-Alvarez, 968; Tom, 976; Gai & Lewinsohn, 98. are bottom-dwelling decapods (Holthuis & Gottlieb, 958; Galil & Lewinson, 98). Molluscs found in the stomach contents were mostly from muddy substrates, with the exception of Polyplacophora and the gastropods Emarginula sicula and Haliotis (Sulculus) tuberculata lameuosa (Mienis, pers. commun.). Fishes constituted only a small fraction of the total stomach contents. They occurred mostly semi-digested and therefore could not be identified beyond the family or order. As seen in Table I, they all belonged to benthic groups such as Blenniidae, Gobiidae and Anguilliformes. DISCUSSION Benthic crustaceans are the main component in the diet of Sargocentron rubrum. According to several authors, other species of the genus have similar feeding habits (McKenney, 959; Randall, 967; Vivien, 973; Woods & Sonoda, 973; Vivien & Peyrot-Clausade, 974; Matthew & Reynold, 978). These authors also stressed the nocturnal feeding habits of holocentrids, although there is some evidence that Sargocentron diadema and Flammeo sammara in Madagascar feed partially in day time (Vivien & Peyrot-Clausade, 974). The present study seems to confirm that S. rubrum feeds predominantly at night. Processa nouveli nouveli, a nocturnal decapod, was not uncommon among stomach contents. Also, as mentioned, S. rubrum occurs in commercial catches at night. Examination of commercial catches indicates that S. rubrum is common at depths of 0-40 m. Live fish were observed near an artificial reef at a depth of 5 m off Shiqmona on the southern outskirts of Haifa. Riedl (I966) observed live individuals of S. rubrum on rocky grounds at depths of 0-40 m off the Anatolian coast of Turkey. Fursa and Movchan (I978) reported specimens of S. rubrum in commercial trawl catches at depths of m off the southwestern coast of India. Thus it seems that in the Indian Ocean S. rubrum occurs in a greater depth range that in the eastern Mediterranean.

10 Vol. 3, 983 FOOD HABITS OF SQUIRRELFISH 03 It is interesting to note that another nocturnal fish of Red Sea origin, Pempheris molucca Cuvier, and also associated with a rocky substrate, has been found recently on the coast of Lebanon (Mouneimne, 979) and Israel (Ben-Tuvia, in press). Ben-Yami and Glaser (974) and Bograd-Zismann (965) suggested the possibility that immigrant species feed mainly on other immigrants. It is difficult to evaluate this hypothesis due to the limited information on invertebrate abundance in the eastern Mediterranean, especially those found on rocky substrates. However, among the 8 decapod species in the eastern Mediterranean (Holthuis & Gottlieb, 958) there were 9 (4.6%) Suez Canal immigrants (Por, 978). Twenty-nine species of decapod were found in the stomach contents of S. rubrum, of which 7 (4. %) were of Red Sea origin. According to Barash and Danin (98), the estimated number of mollusc species in the Levant is 70, of which 70 species (l0%) are Red Sea immigrants (Mienis & Gat, 98). In the S. rubrum stomach contents, 6 mollusc species were found, of which 3 (8.7%) were immigrants. These data indicate that the percentage of immigrant Indo-Pacific species in the S. rubrum diet is similar to their percentage in the Levant Basin. Thus, it seems that S. rubrum is well adjusted to its newly-colonized region in the eastern Mediterranean, feeding on both immigrant and native species. However, it should be stressed that the main biomass of food organisms belongs to the native Atlanto-Mediterranean species (more than 90% of the stomach contents). ACKNOWLEDGEMENTS Yje are grateful to Mr. H. Mienis for the identification of the molluscs and to Dr. M.N. Ben-Eliahu and Mr. A. Diamant for critical reading of the manuscript. We thank Mrs. B. Golani-Appelbaum for the drawing. This study was partly supported by the Fund for. the Encouragement of Research, Histadrut The General Federation of Labour in Israel. REFERENCES Barash, A. and Z. Danin. 98. Mediterranean Mollusca of Israel and Sinai: composition and distribution. Isr. J. Zoo!. 3: Ben-Eliahu, M.N., D. Golani and A. Ben-Tuvia On predation on polychaetes (annelids) by the squirrelfish Adioryx ruber (Holocentridae) with a new polychaete record for the Mediterranean coast ofisrael. Tethys : 5-9. Ben-Tuvia, A Red Sea fishes recently found in the Mediterranean. Copeia : Ben-Tuvia, A Immigration of fishes through the Suez Canal. Fish. Bull. 76: Ben-Tuvia, A. (In press). The impact of the Lessepsian (Suez. Canal) fish migration on the eastern Mediterranean ecosystem. In: T. Platt and M. Apostolopoulou, eds. Mediterranean Marine Ecosystem. Plenum Press. Ben-Yami, M. and T. Glaser The invasion of Saurida undosquamis (Richardson) into the Levant Basin - an example of biological effect of interoceanic canal. Fish. Bull. 7: Bograd-Zismann, L The food of Saurida undosquamis in the eastern Mediterranean in comparison with that in Japanese waters. Rapp. P.-V. Reun., Comm. Int. Exploit. Sci. Mer. Mediterr. 8: 5-5. Fursa, T.I. and Yu. V. Movchan The fish fauna of the southwest coast of India. J. IchthyoL (Vopr. Ikhtiol., Engl. transl.) 8:

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