Dietary Overlap in Spiny Dogfish (Squalus acanthias) and Thornback ...

Dietary Overlap in Spiny Dogfish (Squalus acanthias) and Thornback Ray (Raja clavata) in the Southeastern Black Sea Ekoloji 16, 62, 1-8 2007

Sefa Ayhan DEMÝRHAN Mustafa Kemal University, Faculty of Fisheries, 3103 ANTAKYA Kadir SEYHAN Karadeniz Technical University, Faculty of Marine Sciences, 61530 TRABZON Nuri BAÞUSTA Fýrat University, Faculty of Fisheries, 23119 ELAZIÐ Abstract The food composition and dietary overlap between the spiny dogfish (Squalus acanthias) and thornback ray (Raja clavata) were studied in the Eastern Black Sea. It was found that the food of S. acanthias and R. clavata in the area studied consisted of mainly fish and crustaceans. The availability of prey was found to be the main criterion in the spiny dogfish feeding strategy. In winter, anchovy were the dominant prey for S. acanthias. This reflects that there is a high availability of these prey in the region. The availability of prey items affected the diet composition, the values of diet breadth, the prey similarity and the dietary overlap of the thornback ray and spiny dogfish. The study has shown that the prey similarity index of these species was 38%. The diet of R. clavata was significantly overlapped by the diet of S. acanthias (1.38). However, S. acanthias was observed to have a more unique diet and was insignificantly overlapped by R. clavata (0.36). The overall results indicate that the spiny dogfish is an indiscriminate predator preying upon those species that are most abundant and available in the area and season, and that R. clavata also feed mainly on anchovy and whiting in the winter but shift to crab and Gobius sp., a demersal species common in the area, together with whiting for the rest of the year. Keywords: Black Sea, dietary overlap, food composition, Raja clavata, Squalus acanthias. Güneydoðu Karadeniz'de Mahmuzlu Camgöz (Squalus acanthias) ile Vatoz (Raja clavata) Arasýndaki Besinsel Rekabet Özet Bu çalýþmada mahmuzlu camgöz (Squalus acanthias) ve vatoz (Raja clavata) türlerinin besin kompozisyonu ve aralarýndaki besinsel rekabet araþtýrýlmýþtýr. Bölgede, mahmuzlu camgöz ve vatozun besininin genel olarak kabuklulardan ve balýklardan oluþtuðu tespit edilmiþtir. Mahmuzlu camgözün beslenme stratejisinde ana kriter besinin bulunabilirliðidir. Kýþ mevsiminde ortamda yoðun olarak bulunan hamsi, mahmuzlu camgözün bu dönemdeki ana besinidir. Bu durum, mahmuzlu camgözün besin kompozisyonunu ve diyet geniþliðini etkilediði gibi, dolaylý olarak vatozun besin komposisyonu ile olan diyet benzerliði ve rekabetini de etkilemektedir. Çalýþmada bu iki türün besin benzerliði indeksi %38 olarak bulunmuþtur. Ayrýca vatozun besin kompozisyonu üzerinde mahmuzlu camgözün besin örtüþme deðeri 1,38 olarak bulunmuþtur. Bunun yanýnda daha dar bir diyete sahip olan mahmuzlu camgözün besin kompozisyonu üzerinde vatozun besin örtüþme deðeri 0,36 olarak bulunmuþtur. Sonuç olarak, R. clavata kýþ mevsiminde hamsi ve mezgit ile, yýlýn kalan döneminde yengeç, kayabalýðý türleri, diðer demersal balýk türleri ve mezgitle beslenirken, mahmuzlu camgöz beslenme konusunda seçici davranmamakta ve ortamda bulunan her besin maddesini tüketebilmektedir. Keywords: Besin kompozisyonu, besinsel rekabet, Karadeniz, Raja clavata, Squalus acanthias.

INTRODUCTION The food web of a marine community can be considered as the outcome of and current inter specific competition for available resources (Connell 1983). Estimation of the rate of feeding in addition to stomach content analysis allows calculations of the rate of transfer of food energy No: 62, 2007

through the ecosystem and also the impact on the population dynamics of prey species of a predator. The food availability for a species depends on environmental variability and intra-specific competition (Holt 2002, Sale and Williams 1982). This kind of investigation has gained more importance with a major aim of improving multi1

Ekoloji species assessment and management in fisheries. Schoener (1974) provided information about the niche that they occupy in the local sea area. Spiny dogfish and thornback ray are the most abundant and subject to more research than any other elasmobranch species in the Southern Black Sea (Mater et al. 2005). One of us has also produced a detailed account for biology and ecology of the spiny dogfish (Demirhan 2004) and thornback ray (Demirhan et al. 2005) in the southeastern Black Sea. A recent study carried out in the area revealed that the ratios of elasmobranch species in the total benthic biomass was 16% including Dasyatis pastinaca (Genc 2002). Ciloglu et al. (2002) stated that the ratio of spiny dogfish and thornback ray in the total benthic biomass was 24.21% and 2.17% respectively. Spiny dogfish is a piscivorous and opportunist feeder (Ellis et al. 1996). The thornback ray, however, is known to feed predominantly on invertebrate species, namely crustaceans, (Quiniou and Andriamirado 1979, Cunha et al. 1986, Ebert et al. 1991, Smale and Cowley 1992) although they also feed on fish (Erdem et al. 2001, Morato et al. 2003). Due to the narrow continental shelves and the geo-ecologic characteristics of the Black Sea (Brewer and Murray 1973), both species occur at depths from 25 to 180 m. Despite the overlap in their geographic and bathymetric distributions, little is known about possible feeding competition between these two elasmobranchs. The present study was, therefore, undertaken to study the food and the dietary overlap of these two species in the southeastern Black Sea. MATERIAL AND METHODS Specimens of both species were collected in the southeastern Black Sea by commercial purse seines and gill netts (Fig. 1). Sampling was conducted seasonally, and 52 thornback rays and 176 spiny dogfishes were caught. The numbers of sampled specimens were 35 and 11 in summer, 52 and 30 in autumn, and 67 and 10 in winter for spiny dogfish and thornback rays, respectively. While only six specimens of spiny dogfish were caught in the spring, no thornback rays were caught. Percentages of females were 86.2% for spiny dogfish and 53.8% for thornback ray. While 80% of the female spiny dogfish were in the 120-140 cm length class, 33.3% of the males were in the 110-120 cm length class. The minimum and maximum lengths for spiny dogfish observed was 43.3 and 144.8 cm for females 2

S. A. DEMÝRHAN, K. SEYHAN, N. BAÞUSTA and 38.1 and 123.0 cm for males, respectively. Thornback rays ranged between 34.3 to 88.2 cm for females and 48.0 to 95.0 cm for males. While 89.3% of the female thornback rays were in the 120-140 cm length class, 31.8% of the males were in the 70-80 cm length class. Stomachs with contents were placed in numbered plastic bags and frozen for subsequent analysis. In the laboratory, whenever possible, prey were visually identified to species level and unidentified remains noted. The stomach contents were weighed and the volumes of the stomachs were measured to the nearest g and mL, respectively. Signs of vomiting were not observed in the specimens (Hureau 1970, Hyslop 1980). However, it was difficult to determine this situation since the specimens were taken from the commercial fisheries. Stomach contents were analyzed with regards to the importance of prey in the diet of the spiny dogfish and thornback ray by using the methods (eq. 1-2-3) proposed by Hureau (1970), Hyslop (1980), Cortes E (1998), Hickley et al. (1994), Hansson (1998) and Gokce et al. (2005). All formulas are as follows:

where Oi% is the percent frequency of occurence of prey i, FOi is the frequency of occurrence of prey i, NS is the total number of stomachs examined, Ni% is the percent by number of prey i, Ni is the total number of prey i, Np is the total number of prey, Wi% is the percent by weight of prey i, Wi is the total weight of prey i, Wp is the total weight of prey. The percentage of index of relative importance (IRI%) (eq. 4), feeding coefficient (Q) (eq. 5) and percentage of predominance value (PVi%) (eq. 6) were used to evaluate the relative importance of various prey types in the diet and to provide a quantitative description of stomach contents. Where IRIi is the index of relative importance of prey i, Q is the feeding coefficient and PVi is the predominance value of prey i. Diet breadth indices (Bx, By) (eq. 7) (Shannon and Weaver information statistics) were calculated to No: 62, 2007

Dietary Overlap in Spiny Dogfish (Squalus acanthias) and ...

illustrate the range of the available resources for both species (Krebs 1989).

Where Bx and By are the dietary breadth of the predator species x and y. B values vary from 1.0 (when the species uses one resource category exclusively) to the number of all resource categories (when it uses all categories in equal proportions). A modified Schoener's index, called the Percent Similarity Index (PSI) (eq. 8) and the MacArthurLevins' method were used to quantify diet overlap between the two species. The PSI is the sum of the proportion of individual prey species in common between the two predators, and is calculated according to Morisita (1959).

Where p is the proportion of prey category j in predators x and y. The PSI ranges from 0 to 100%, where 0% indicates no overlap and 100% indicates complete overlap in the diet of the two predators (low similarity 0-24%, moderate 25-40%; high 5074%, very high 75-100%., Hyslop 1980). According to Wallace and Ramsey (1983), overlap values > 0.6 should be considered as biologically significant. The MacArthur-Levins' method (MRS, MRS) is an asymmetrical comparison and calculated using the following equations (MacPherson 1981).

Where MRS is the amount of overlap on R. clavata by S. acanthias, MRS is the amount of overlap on S. acanthias by R. clavata, PIR and PIS are the proportions that food resource i contributes to the diets of species R. clavata and S. acanthias, respectively. Evaluations were performed with regards to whole year (WY), winter (W) and excluding winter (EW), separately. RESULTS A total of 176 dogfish and of 52 thornback rays No: 62, 2007

Ekoloji were captured during 2001-2003, of the examined stomachs, 35 (70%) R. clavata and 65 (37.2%) S. acanthias stomachs were empty. The main prey items found in the stomachs of the thornback ray were anchovy (Engraulis encrasicholus, Linnaeus 1758) and whiting (Merlangius merlangus euxinus, Nordmann 1840) (62.5%), but shrimps (Upogebia pusilla, Pategna 1792, Crangon crangon, Linnaeus 1758) and crab also contributed to the diet of R. clavata (Fig. 2). The spiny dogfish in the southeastern Black Sea, on the other hand, fed on a variety of fish species, however the main fish prey was also anchovy (E. encrasicholus) (94%). A new born baby dogfish (S. acanthias) was also noticed in their diet (Fig. 2). In addition, feathers, gravel, nylon bags, straws, leaves, cetacean (intestines, skin, fin, bone) and spiny dogfish pieces were found in some stomachs of the spiny dogfish. A detailed account is given in Table 1. When the data was analyzed by taking the feeding coefficient (Q) into account, it was revealed that the importance of prey differed throughout the year (Table 2). For example, anchovy was found to be the main prey only in winter while whiting was the principal prey for S. acanthias for the rest of the year. For R. clavata, not only anchovy, but also whiting was found to be the main prey all year around. In addition crab was also found to be an important prey item. The dietary breadth is a quantitative measure of the specifics of a species' diet (Krebs 1989). The estimated value for R. clavata was higher than that of S. acanthias, (4.84, 2.45 and 4.60 for R. clavata in the whole year, the winter and the except winter periods respectively; 1.25, 1.19 and 3.44 for S. acanthias in the whole year, the winter and the except winter periods respectively) reflecting that R. clavata tend to use a broader range of available resources in all seasons of the year. It was also found that the Prey Similarity Index (PSI) estimated for S. acanthias and R. clavata were different for the whole year except in winter (Table 3). The MacArthur-Levins' Index of dietary overlap was also calculated. A value of 0.7 or higher is considered significant (MacPherson 1981). Estimated dietary overlap values between the spiny dogfish and thornback ray were found to be different for the whole year except in winter. The diet of R. clavata was significantly overlapped by S. acanthias for the whole year (Table 3). S. acanthias was, however, observed to have a more unique diet 3

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Fig. 1. Sampling area.

Fig. 2. Food compositions of S. acanthias and R. clavata by prey groups (WY; whole year, W; winter, EW, except winter).

than R. clavata (Table 3) and it was insignificantly overlapped by R. clavata throughout the year. DISCUSSION This study shows that the thornback ray and spiny dogfish prey upon anchovy, whiting, shrimp and crab, and that the spiny dogfish is an indiscriminate predator preying upon whatever species are most abundant and available in the area and at the time. This is a sign of the opportunistic feeding strategy of the spiny dogfish. The availability of prey items affected the diet composition, the values of diet breadth, the prey similarity and the dietary overlap of these species. The investigation showed that many stomachs of both species examined were empty. This is a common observation made by several other researchers (Aasen 1961, Holden 1966, Bonham 1984, Ellis et al. 1996). Since spiny dogfish have an intermittent feeding strategy rather than vomiting upon capture, behavioral changes related to the fullness of the stomach, or rapid digestion (Aasen 1961, Holden 1966). Most other researchers stated that, demersal and pelagic fishes and crustacean are important in the food compositions of the thornback ray and spiny dogfish in different ratios (Aasen 1961, Holden 1966, Bonham 1984, Ellis et al. 1996) and it resembles our findings with the recent study. While the ratios of those prey groups were 4

S. A. DEMÝRHAN, K. SEYHAN, N. BAÞUSTA similar for both species for the whole year in this study, the ratios of pelagic fishes (i.e. anchovy) get more important in winter especially for the spiny dogfish. For this reason data was evaluated for the whole year (WY), winter (W) and except winter (EW), separately. The main reason of variation in the diet composition of the spiny dogfish and thornback ray is seasonal distribution and the migration of anchovy (Erkoyuncu and Ozdamar 1989) in the Black Sea. The prey similarity index was relatively high for the two species, although, the dietary breadth indices of the two species were relatively low in winter. However, the diet of the thornback ray was significantly overlapped by the diet of the spiny dogfish for the whole year (1.38) and in winter (1.35). On the other hand, the diet of the spiny dogfish was insignificantly overlapped by the diet of the thornback ray for all periods (W, EW, WY). Spiny dogfish and thornback rays mostly feed upon anchovy in the winter period in different ratios in the southeastern Black Sea. Several researchers stated that, pelagic fish species play a more important role in the diet of the spiny dogfish (Bonham 1984, Ellis et al. 1996). Moreover, the spiny dogfish are capable of rising to the surface to prey upon species found in surface waters like euphasiids (Beamish et al 1992, Siegel 2000). It is expected that pelagic fish species are important food items of the spiny dogfish in the Black Sea. Purse seines catch mainly anchovy in addition to spiny dogfish in the winter. Samples which had stomach full with anchovies were taken from the purse seines. It can be concluded that the specimens that remained in the purse seines had filled up their stomachs with the congested anchovy in the purse seines within 1-2 hours. This might be interperated as the increasing importance of anchovy in the diet composition of the spiny dogfish. Our observation indicated that these specimens had completely digested (vertebrates of anchovies remained), partly digested (there were some meat on the vertebrates of anchovies) and almost no digested anchovies in similar proportions in almost all stomachs of the samples of the spiny dogfish. Because spiny dogfish could not digest the anchovy completely in 1-2 hours. Spiny dogfish must have been preying upon the anchovy schools before they were caught and filled up their stomachs with congested anchovy when they remained in the purse seines. From the morphological point of view, rays can No: 62, 2007

Table 1. Food compositions of R. clavata and S. acanthias (WY: whole year, W: winter, EW: except winter).


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Ekoloji Table 2. Importance of prey items by Q.

"pp, principal prey; sp, secondary prey; op, occasional prey; rp, rarely prey"

Table 3. Dietary overlap values, prey similarity indexes, N% and O% for shared preys by S. acanthias and R. clavata.

not feed in the water column and are obliged to feed upon demersal species such as fishes and crustaceans. Many researchers stated that rays and skates consumed pelagic fish species (Beretovsky 1989, Ellis et al 1996). However, it was suggested 6

that rays and skates could only prey upon pelagic fishes traumatized by fishing nets (Beretovsky 1989). The present study supports Beretovsky's (1989) results in that there is a scarcity of anchovies found in the stomachs of thornback rays. No: 62, 2007


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It is difficult to make a definite decision about the feeding strategy and interaction between the thornback ray and spiny dogfish because of the scarcity of samples. However, it is important that,

this is the first study about food composition and feeding competition of the two elasmobranchs species in the Anatolian coast of the Black Sea.

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MacPherson E (1981) Resource partitioning in a Mediterranean demersal fish community. Mar. Ecol. Prog. Ser. 4, 183-193. Mater S, Kaya M, Bilecenoglu M (2005) Turkey Marine Fishes-1, Cartilaginous Fishes (Chondrichthyes), Ege University Publication, Izmir. Morato T, Solà E, Grós MP, Menezes G (2003) Diets of thornback ray (Raja clavata) and tope shark (Galeorhinus galeus) in the bottom long line fishery of the Azores, Northeastern Atlantic. Fish Bull. 101, 590-602. Morisita M (1959) Measuring of interspecific association and similarity between communities. Mem. Fac. Sci. Kyushu Univ. Ser. Env. Biol. 3, 65-80. Quiniou L, Andriamirado GR (1979) Variations du régime alimentaire de trois espèces de raies de la baie de Douarnenez (Raja montagui Fowler, 1919; Raja brachyura Lafont, 1873; Raja clavata L., 1758). Cybium 7, 27-39. Sale PF, Williams DMcB (1982) Community structure of coral reef fishes: are the patterns more than those expected by chance? American Naturalist 120, 121-127. Schoener TW (1974) Resources partitioning in ecological communities. Science 185, 27-39. Siegel V (2000) Krill (Euphausiacea) life history and aspects of popilation dynamics. Can. J. fish Aquat. Sci. 57, 3, 130-150. Smale MJ, Cowley PD (1992) The feeding ecology of skates (Batoidea: Rajidae) off the Cape south coast, South Africa. S. Afr. J. Mar. Sci. 12, 823-834. Wallace H, Ramsey JS (1983) Reliability in measuring diet overlap. Can. J. Fish. Aquat. Sci. 40, 347351.

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