original scientific paper UDK 597.5:591,13(262.3-1 1) FOO D AN D FEEDING HABITS O F THE DAMSELFiSH CHROMIS CHROMIS (TELEOSTEI: POMACENTRIDAE) IN THE EASTERN ADRIATI C Jakov DULČiČ Ph.D., fisheries biologist, Institute of Oceanography and Fisheries - Split, HR-21000 Split, Set. i, Meštroviča 63 dr., ribiški biolog, !OR, HR-21000 Split, Set. 1. Meštroviia 63 ABSTRACT The stomach contents of 964 damseifish Chromis chromis collected in the eastern central Adriatic in 1992 and 1993 were examined to assess the diet, as influenced by season and fish size, Damseifish is carnivorous from the juvenile stage onward, feeding on a narrow range of plankton and benthic prey items, Higher intensity of feeding activity in spring could be related to temperature and/or gonadal maturation. During all seasons copepods constituted the most important food resource by weight, number and frequency of occurrence. Appendicularia and cladocerans were the second most important food category. Dietary overlap was relatively high, indicating that the feeding spectrum of damseifish changed little across seasons, but for size groups was small, indicating greater changes in feeding spectrum. Ključne besede: črnik, Chromis chromis, prehrana, prehranjevalne navade, ceponožci, vzhodni Jadran Key words: damseifish, Chromis chromis, food, feeding habits, copepods, Eastern Adriatic INTRODUCTION Despite its abundance, very little is known about the trophic ecology of damseifish in the Mediterranean Sea. The damseifish, Chromis chromis {Linnaeus, 1758) is The present study deals with food and feeding habits of a small fish found in shoals in mid-water above or near the damseifish off the Eastern Adriatic. The purpose was rocky reefs or above sea grass (Posidonia) meadows at to examine the feeding habits and intraspecific resource depths ranging from 3 to 35 m. It occurs in the partitioning across seasons and during developmental Mediterranean and from Portugal southwards to Angola life stages of damseifish in the Eastern Adriatic. (Quignard & Pras, 1986). In the Eastern Adriatic, the damseifish is abundant MATERIAL AND METHODS (Grubišič, 1982; Milišič, 1994), but it is of no commer­cial value along the eastern coast (except on the central A total of 964 specimens of damseifish were ob-Adriatic islands of Solt.a, Hvar, Korcula and Lastovo, tained during four seasonal beach seine survey cruises, where it is much appreciated). In coastal fishery of Dal-from summer 1992 to spring 1993. Samples were taken matia, damseifish form a small but significant compo-near the island of Trstenik in the central Adriatic (Fig. 1}. nent of the coastal beach seine and gill net catch that is Damseifish were fixed in 4% formalin immediately after used as delicious food and as bait for lobsters. We have capture. The fish were processed promptly after no new data on catch, but. Grubišič (1982) reported that collection. Processing included measurements and it is around 30 tons per year. weighing to nearest 0.1 cm and 0.01 g respectively and There are some data about the biology and ecology gut removal prior to which both ends of the stomach of this species from the eastern Adriatic. Dulčič et at. were tied off. The contents of the dietary material were (1994a) presented data on the length-weight relationship identified to the specific level where possible, but most in damseifish during spawning in the Eastern Adriatic. items were identifiable only to the generic level. Pres­Dulčič et al. (1994b) analysed the vertebra! number of ence of inorganic matter and detritus in the stomachs damseifish. Age, growth and mortality of damseifish was recorded, but excluded from the analysis. After were presented by Dulčič & Kraljevič (1995). identification, preys were weighed to the nearest 0.01 g. Jakov DULČl C FOO D AN O FEEDING HABITS O f TH E DAMSELEISH, ..., 31-36 Fig. 1: Location of sampling station in the eastern central Adriatic, where damselfish (Chromis chromis) were collected (Trstenik Island). Slika 1: Zemljevid obravnavanega območja z označeno vzorčevalno postajo (otok Trstenik), kjer so bili ulovljeni črniki (Chromis chromis)> The contribution of the prey categories to (he diet of damselfish was calculated as (1) the percentage of wet weight (Cw) of a prey category (pooled) to the weight of the total stomach contents, (2) the percentage abun­dance (Cn) of individuals of a prey category to the total number of prey individuals in the stomachs, (3) the fre­quency of occurrence (f) of stomachs in which a prey category occurred to the total number of stomachs ex­amined (Hyslop, 1980). George & Hadley (1979) em­ployed the "relative importance index" (Rl) which is based on the "absolute importance index" (Ai) as fol­lows: Al = % frequency occurrence + % total numbers + % total weight; Rl = 100 Al / niL A[, where n is the number of i different food types. Seasonal variations were analyzed using Fischer's least significant difference (LSD) test (Zar, 1984). The analysis of changes in feeding habits in different seasons and in different length classes was performed by the use of the full ness index (Hureau, 1970): %jr = fullness in­dex: weight of digested food/fish weight x 100. Proportional food overlap between size classes and seasons for the species was calculated using the overlap index of Schoener (1970): Cih = 1-0. 5 ® Pij - Phj), where Pij and Phj are the proportions of prey j found in the diets of groups i and h respectively. This index has a minimum of 0 (no overlap of prey) and a maximum of 1 (all items in equal proportions). Schoener's index values above 0.60 are usually considered to be "biologically significant" (Zaret & Rand, 1971; Wallace, 1981), in­dicating a high dietary overlap (Langton, 1982). RESULTS AND DISCUSSION Fish lengths in the sample ranged from 8 to 1 34 mm caught (Fig. 2). Data sampled in 3 areas were aggre­gated for the analysts since there was no significant dif­ference between them (ANCOVA). The specimens were divided into two size groups, to examine feeding habits of the fish developmental stages. Group 1 comprised fishes smaller than 65 mm (juvenile stage) and Group 2 fishes longer than 65 mm (adult stage). The proportion of empty stomachs among fish up to 65 mm long is 6.9%, while this proportion in longer fish is 5.0%. Feeding intensity expressed by the fullness index (jr) was higher in smaller (jr—6,83) than in larger fish (Jr-3.80). In Group 1, polychaetes, ostracods, copepods and mysids constitued the bulk of the diet, while copepods, appendicularins and ciadocerans were dominant in Group 2 (Table 1). Stomachs of larger individuals con­tained ail mentioned prey taxa ingested by smaller fish, but in different proportions. Copepods were the do­minant prey of damselfish in both size-classes, Clause-ca/anus pergens being the dominant species. As fish grew older there was a difference in the "relative index" (Rl) of polychaetes, copepods, ostracods and mysids. Polychaetes exhibited a greater presence in the sto­machs of smaller fish, corroborating the view that small damselfish select prey of low mobility. n — nI I t n H Í1 J—ill | ' ' i 'Hnn ] I | 1 L-^^f.,,,,^ , I 1 L .1 — r | ^ t M 30 tO 51 SO » SO <13 )CC !!0 IÎD 130 UG TOTAL LEfv&lH [mm) Fig. 2: Length frequency distribution of damselfish (Chromis chromis) collected in the eastern central Adriatic for dietary studies in 1992 and 1993 (n = 964). Slika 2: Velikostna porazdelitev dolžine črnikov (Chro­mis chromis), ulovljenih v vzhodnem srednjem Jadranu v obdobju 1992-1993 (n = 964). ANNALES <>/'96 lakov PUlClČ : FOO D AN D FEEDING HASH'S O f TH E DAMSELFISH, ., H (-3 6 Siz e groups m m > mm SeJ'.tm Winter Summer Con ! rib lit ion of the f A I Ri f A l RI O/ntnb'.itli-yn 17.t the ( At RI f C w C « C-w ci 5 c w C, v At RI prey allegorie s prey categories Polych.ieta 34.3 7.7 30. S 72,S 13.03 2 4 0.1 0.5 3 0.25 Poiydwt a 1-1,1 0.2 1 ,3 15.6 2.49 Appendicular « 76.2 27 13.8 117 9,93 Appendicular ia 53.8 22.1 2.7.5 103.-1 19.72 83.6 32.) 16.7 138,4 22,1! Ostracocla 3(1.9 27,4 19,5 85.8 15.<12 10.8 0.3 3.2 14.9 1.27 Osiraearb 11.5 0.0 3.2 15.5 2.48 Copepocta 94.7 55,6 12.7 163 29.30 93.1 37 7 2T..7 156.5 13.29 Copepocta 100 58.2 33.8 192 36.61 75.6 34.2 24 6 134.4 21.SO Paracalanus parvus 76.2 7.6 SA 89.2 7.57 Ckripedia truiuplii) 3.7 0.7 2 6.4 1 .02 Claiisocatanus per gem 36.8 23 S 3 65.1 11.70 51.7 10,1 6.1 67.9 5.77 Decapods (iarvae) 25.2 5.6 7.4 38.2 6.10 C. furca(us 21.1 15 3.4 39.5 7.10 37.5 6,2 4.3 47.6 4, M iViy.^ddi-.ej 6.2 0.2 2.1 8.5 1.36 C.helgolandictis lî. G 1.1 I. I 13.8 5.17 Cbdocer a 100 12.7 26.8 139.5 26.tO »4.1 22.4 12 i 18.5 18.9.3 Cparapergens l 5,6 5,2 2.9 23.7 2.01 Gastropoda 11.8 0.9 17 29.7 47 4 C.tetwicvrnis 19 TO.S 2,-4 31.9 5.73 3.3 0.1 0.1 3.5 0.30 (larvae) Eitcaliinus efangatus 1 OS 5 1.2 16 7 3 2.3 0.1 0.1 2.5 0.21 Sivatvia (larvae) S.9 0.9 7.3 (4.1 2.2.5 Eulerpina acutiformte 65 mm % of empl y stomachs 6.9 5.0 % Jr 6.83 3.80 Table 1: Contribution of the prey categories for dam-Table 3; Fullness index (Jr) in specimens analyzed by selfish stomach contents according to size groups. seasons. Tabela 1: Delež posameznih kategorij plena v želodcih Tabela 3: Hureaujev indeks (Jr) primerkov; raziskanih v črnika glede na velikost. različnih letnih časih. 33 jakov DULÔC : FOO D AN D FEEDING HABITS OF THE DAMS ELFISH 31-36 Season Winter Spring Summer Autumn Winter 0.70 0.67 0.93 Spring 0.80 0.71 Summer 0.69 Autumn Size group 8 - 65 mm > 65 mm 8 - 65 mm 0.58 > 65 mm Table 4: Proportional food overlap coefficients (Scho­ener index) of damselfisb between seasons. Tabela 4; Količnik prekrivanja v prehrani (Schoenerjev indeks) črnika v posameznih letnih časih. Feeding intensity was lowest in winter, indicated by the higher frequency of empty stomachs in each group {14% for Croup 1 and 11 % for Group 2). Copepods constited the bulk of diet throughout the year (Table 2), exhibiting their highest values by number during spring and summer. Cladocerans and Appendicu­lar ia were the second important food categories. They were eaten regularly during all seasons. Seasonal changes in Rl were examined to detect which prey accounted for the differences in the diet, This analysis indicated a great importance of copepods in all seasons. Food quantity in analyzed guts, expressed as the fullness index (Jr), was highest in spring (jr = 5.67) and a significant drop was recorded for winter (Jr = 1.91) (Table 3). Fischer's LSD test indicated that the mean fullness index was significantly higher in spring and summer. The application of ANOV A and multiple range tests to the seasonal data indicated significantly higher values in spring (ANOVA: F = 12.424, P <0.001). Values of Schoener's (1970) index of dietary overlap were obtained from a comparison (by weight) between the different size groups (0.58) and seasons (Table 4), Almost all the values were > 0.60, indicating high die­tary overlap. Thus, the feeding spectrum of damselfish depends little across season of capture. The small vari­ations of the principal prey items between the different seasons contributed to the high level of inter-season proportional overlap. Damselfish in the eastern Adriatic fed primarily on crustaceans, mostly copepods (such as Paracalanus parvus, Clausocalanus pergens and Centropages typicus) and cladocerans (Podon intermedius), but also con­sumed Appendicular!», Gastropoda (larvae) and Bivalvia (larvae), fish eggs and fish larvae, mainly at larger lengths. Polychaetes, Ctrripedla (nauplii), Mysidacea and Decapoda (larvae) were also occasionally found in the stomachs. These results are generally in accordance with the observation of Duka & Shevchenko (1980) off the Mediterranean coast of island Lampedusa and for damselfish from the Black Sea. Same authors mentioned that copepoda (Calanoida, Cyclopoida - 15 species) were the most abundant food items, that Appendicularia (Oikopleura dioica) ranked second in the Mediterra­nean, and that damselfish eggs and Appendicularia (Oikopleura dioica) were the most abundant food items in the Black Sea. Although no quantitative data on prey consumption of damselfish were given, it is not possible to compare the data on that basis. Mapstone & Wood (1975) revealed that, damselfish feeds both on plank­tonic. and benthic organisms; eight out of 11 individuals contained predominantly planktonic and three pre­dominantly benthic organisms in the Azores. The stomachs of both size groups were significantly fuller in spring and summer, while the lowest feeding intensity coincided with winter. Many factors could re­sult in the reduction of feeding activity in fish (Nikolsky, 1976). Many of the demersal fishes show a decrease in the feeding rate as the temperature drops (Tyler, 1971), In the study area, the lower temperature of the water oc­curs during winter (February) and beginning of spring (Zore-Armanda et. ah, 1991). Because of the reduced abundance of prey and the lowered metabolism of the fish, predation on plankton and benthos was probably at a minimum during winter. Regner (1985) presented, for the central Adriatic, that copepods showed larger num­ber of annual maxima predominantly during the warmer part of the year: in spring, summer and autumn. This oc­currence of a larger number of maxima may be due either to natural fluctuations or to the enrichment of coastal area by nutrients (eutrophication) as well as to the sufficient food available over a larger part of the year. Favourable environmental conditions during the warmer months and abundant food supply support the expanded fish community without competitive interac­tions. However, the effect of temperature may be con­founded with the effects on other abiotic factors and/or in change in food availability (Worobec, 1984). Warren & Davis (1967) discussed the profound effects of tem­perature and seasons on food consumption rates, More food is consumed in summer than in winter, this was demonstrated (Davis & Warren, 1965) from the experi­ments with Coif us perplexus. Reproduction, which takes place at the end of spring and during summer (Duičič & Kraljevič, 1995), seems to have effect on feeding intensity (gonadal maturation). Feeding behaviour of most of fish species considerably oscillates during the year as a consequence of a physi­ological changes during reproduction, jardas & Pallaoro (1991) found that feeding intensity of Scorpaena porcus expressed by the index of gut fullness showed markedly lower values during spawning, whereas it was at almost the same level during the rest of the year, with slight in­tensity increase in the postspawning period. Similarly to damselfish, high degrees of stomach fullness were re­ported for other demersal fish in the same area, such as |,ikov DtJlCl é FOO D AN D FEEDING HABITS O f THE DAMSELFISH, ,.., 31-M fig. 3: School of Damselfish (Chromis chromis) (Photo: M. Richter). Slika 3: fata irnikov (Chromis chromis) (Foto: M. Richter). Scorpaena porcus (jardas & Pallaoro, 1991), indicating an abundance of food in this region even though this region contributes to oligotrophy area according to Buijan & Zore-Armanda (1976), The abundance of food in this region is connected with the upwelling in the area of Palagru^a sill which is in vicinity of the studied area (Regner ef a/,, 1987), This occurs certainly more strongly during years with increased Mediterranean in­flow at the time of strong advection of the intermediary water and also during the upwelling periods in spring and summer (Buijan, 1965). In the open central Adriatic the zooplankton (dry weight) shows a distinct spring maximum in March and April (Vufietid, 1973). Upwel­ling may be caused later in the spring-summer period by dominant coastward wind direction (the maestrai). The spring maximum of the zooplankton is characterized by the presence of typical deep sea species; the maximal population densities at the beginning and by the end of summer are attained by the typical neritic species (VuCetiC, 1 973). The maximal quantities of zooplankton occurs firstly in the open sea and then farther towards the coast. Dietary overlap is lower between summer and win­ter, when the metabolic demands are higher than for the rest of the year. This fact indicates that intraspecific competition for food between fish of the two groups is small, probably because of the different bathymetrical distribution of damsetfishes at different size. The study of the bathymetrical distribution of the two groups revealed that younger specimens tended to inhabit smaller depths (DulCic, unpublished data), Fig. 4: Male and female damselfish. The male is waiting for the proper moment to fecundate the eggs (Photo: M. Richter). Slika 4: Samec in samica črnika. Samec čaka, da se samica umakne, da lahko oplodi !zmetana jaca (Foto: M. Richter). POVZETEK Črnik Chromis chromis (Linnaeus 1758) je majhna riba, ki jo najdemo v plitvih vodah nad ali v bližini čeri ali pa nad travniki morske trave pozejdonke (Posidonia oceani ca), in sicer v globini od 3 do 35 metrov. Živi v Sre­dozemskem morju in v vodah južno od Portugalske do Angole (Quignard & Pras 1986). V vzhodnem Jadranu ječrni k številčen (Crubišič, 1982; Milišič 1994), vendar tam komercialno ni zanimiv (razen na otokih Šol ti, Hvaru, Korčuli in Lastovem v srednjem Jadranu, kjer je zelo cenjen). V dalmatinskem obalnem ribištvu so črniki majhen, a pomemben sestavni del ulova z mrežami, uporabni predvsem kot slastna jed in vaba za jastoge. Da bi ocenili, s čim se črniki prehranjujejo glede na različne letne čase in velikost, je bila raziskana vsebina želodcev 964 osebkov, ujetih v vzhodnem srednjem Jadranu v letih 1992 in 1993. Črnik je mesojeda riba že od svojega mladostnega stadija naprej, hrani pa se le z določenimi planktonskimi in bentoškimi organizmi. Večjo prehranjevalno intenzivnost v spomladanskem času bi lahko pripisali temperaturnim spremembam in dozorelosti Jakov OULČiČ : K>O D AN D FEEDINC HABITS OF "J H F DAM5FEF1SH, ..., 31-36 spolnih žlez. Po biomasi, številu in pogostosti pojavljanja v celoletnem obdobju so bili ceponožci najpomembnejši vir hrane. Drugi najpomembnejši prehranjevalni vir so bili repati plaščarji in morske bolhe. Prehransko prekrivanje je bilo razmeroma izrazito, kar pomeni, da so razlike v prehranjevalnem spektru črnikov prek vseh štirih letnih časov majhne, medtem ko je bilo za velikostne skupine neznatno, kar kaže na večje spremembe v prehranjevalnem spektru. REFERENCES Buijan, M. (1965) Anomalies of temperature and chlonnity of sea water on the station StonCica (middle Adriatic}. Pomorski zbornik 6: 949-995. Buijan, M. & Zore-Armanda, M. (1976) Ocea no-graphical properties of the Adriatic Sea, Oceanogr. Mar. Biol. Ann. Rev. 14: 11-98. Davis, G.E. & Warren, C.E. (1965) Trophic relations of a sculpin in laboratory stream communities. /, Wildl. Mgmt. 29: 846-871, Duka, L.A, & Shevchcnko, N.F. (1980) Morphology and nutrition of Chromis chromis (Linne) in the Medi­terranean and Black Seas. Ekhol. Morya 3: 26-33. (in Russian) Dulcic, J., Kraijevic, M. & Cetink, P. (1994a) Length-weight relationship in damselfish (Chromis chromis L. 1758) from the eastern Adriatic during spawning. Acta Ichthyologica et Piscatoria 2: 147-154. Duldc, J., Cetinid, P. & Kraijevic, M. (1994b) Analysis of the vertebral number of damselfish Chromis chromis (L.) in the central Adriatic, Acta Ichthyologica et Piscatoria 2: 141-146. Dulcic, J. & Kraijevie', M. (1995) Age, growth and mortality of damselfish (Chromis chromis L.) in the eastern middle Adriatic. Fish. Res. 22: 255-264. George, E.L & Hadley, W.F. (1979) Food and habitat partitioning between rock bass (Ambloplites rupestris) and smallmouth bass (Micropterus dolornieui) young of the year. Trans.Am.Fish.Soc. 108: 253-261. Grubisic, F. (1982) Ribe, rakovi i Skoljke jadrana. !TRO Naprijed, Zagreb-GRO Liburnija, Rijeka. 240 p. Hureau, J.C. (1970) Bioiogie cornparee de quelques Poissons antartiques (Nototheniidae). Bull. Inst. Oce­anogr. Monaco 68: 89p. Hyslop, EJ. (1980) Stomach contents analysis - a review of methods and their application, j. Fish. Biol. 17: 411­429, Jardas, 1. & Pallaoro, A. (1991) Food and feeding habits of black scorpionfish (Scorpaena porcus L. 1758) (Pis­ces: Scorpaenidae) along the Adriatic coast. Acta Adriat. 32: 885-898. Langton, R.W. (1982) Diet overlap between atlantic cod, Cadus morhua, silver hake, Merluccius bilinearis, and fifteen other Northwest Atlantic finfish. Fish. Bui I. U.S. 80: 745-759. Mapstone, G,M. & Wood; E.M, (1975) The ethology of Abudefduf luridus and Chromis chromis (Pisces: Poma­centridae) from Azores. j.Zool.London 175: 179-199. MiliSiC, N. {1994) Sva riba jadranskog mora. NfVA-Split. Nikolsky, G.V. (1976) The Ecology of Fishes. London. Academic Press, Qurgnard, j.P. & Pras, A. (1986) Pomacentridae. In: Fishes of the north-eastern Atlantic and Mediterranean. Whitehead P.J., Bauchot M.L, Hureau j.C., Nielsen j.& Tortonese E, ii, UNESCO, United Kingdom. Regner,, D. (1985) Seasonal and multiannual dynamics of copepods in the middle Adriatic. Acta Adriat. 26: 11­ 99. Regner, S., Regner D., Marasovii, l„ & Krsinid, E. (1987) Spawning of sardine, Sardina pilcbatdus (Wal­baum, 1792), in the Adriatic under upweiling con­ditions. Acta Adriat. 28:161-198. Schoener, T.W. (1970) Non-synchronous spatial overlap of lizards in patchy habitats. Ecology 51; 408-418. Tyier, A.V. (1971) Monthly changes in stomach contents of demersal fishes in Passamaquoddy Bay (N.B.). Fish.Res.Board Can. Techn.Pap. 288: 114 p, Vucetid, T. (1973) Zooplankton and circulation pattern of the water masses in the Adriatic, Neth.J.Sea Res. 7: 112-121. Wallace, R.K. (1981) An assessment of diet overlap indexes. Trans.Am.Fish.Soc. 110: 71-76. Warren, C.E. & Davis, G.E. (1967) Laboratory studies on the feeding bioenergetics and growth of fish. In: The biological basis of freshwater fish production. Eel. Gerking S.D. Blackweii Scientific Publications, London: 123-135. Worobec, M.N. (1984) Field estimates of the daily ration of winter flounder Pseudopleuronectes america­nus (Waibaum) in a southern New England salt marsh. j.Exp.Mar.Biol.Ecol. 77: 183-196. Zar, J.H. (1984) Biostatistical analysis. 2nd edn. Pren- tice-Hall, Englewood Cliffs, Nj. Zarrel, T.M. & Rand, A.S. (1971) Competition in tro­pical stream fishes: support for the competitive exclu­sion principle. Ecology 52: 336-342. Zore-Armanda, M., Bone, M., Dadk, V., Morovic, M., Ratkovic, D., Stojanosld, L. & Vukadin, I. (1991) Hydrographic properties of the Adriatic Sea in period from 1971 through 1983. Acta Adriat. 32: 6-554.