Iranian Journal of Fisheries Sciences 15(4) 1616-1623 2016

A study of food consumption of the deepwater Goby, Ponticola bathybius (Kessler, 1877), during spring migration in the southern Caspian Sea

Tajbakhsh F.1; Abdoli A.A.2*; Rajabi Maham H.3; Hashemzadeh Segherloo I.4; Kiabi B.1

Received: January 2016 Accepted: May 2016

1-Department of Marine Biology, Faculty of Biological Sciences, Shahid Beheshti University, G. C., Tehran, Iran 2-Department of Biodiversity and Ecosystem Management, Environmental Sciences Research Institute, Shahid Beheshti University, G, C, Tehran, Iran 3-Department of Zoology, Faculty of Biological Sciences, Shahid Beheshti University, G. C., Tehran, Iran 4-Department of Aquaculture, Faculty of Natural Resources and Earth Sciences, University of Shahre Kord, 115, Iran *Corresponding author's email: [email protected]

Keywords: Gobiidae, Feeding strategy, Modified Costello method, Caspian Sea, Iran.

Introduction great consumers of food resources and the The Gobies exhibit a main role in the considerable competitors for other species general production of the Caspian Sea due (Corkum et al., 2004). According to Miller to their species diversity and unexploited (2003), fish are as dominant prey for larger stocks. So, of the 80 fish species known specimens of P. bathybius, while from Iranian part of the Caspian Sea, 10 of Crustacea are main prey for smaller them are gobies (Abdoli et al., 2012). The specimens (Gaibova and Ragimov, 1970). deepwater goby, Ponticola bathybius Also, Kalantarian et al. (2013) found out (Kessler, 1877), Gobiidae, is a native that this fish feed mainly on N. pallasi (in species in the Caspian Sea which settles on species N. pallasi instead of N. fluviatilis sandy and shelly substrates and, in a few in the Caspian Sea (revised by Neilson and numbers, on firm silt down to 75 meters Stepien, 2011) in all seasons and age (Miller, 2003). The presence of predators groups (5-8 years). New habitats can be as such as Acipenseridae and prey items as an effective factor for changing the food Clupeonella sp. could be effective in the patterns in fish (Brander et al., 2013). abundance of gobies (Kalantarian et al., According to Liasko et al. (2012), the 2013). Gobies fishes are known as the abundance of food resources was 1617 Tajbakhsh et al., A study of food consumption of the deep water Goby Ponticola bathybius … considered as important environmental since they move to coastal waters earlier factors even leading to the morphological than the females for reproduction. Total variations in fish. Several studies pointed length (TL) of the fish were measured by a out that Ponto-Caspian gobies display an caliper to the nearest 1 mm and weighed to opportunistic feeding strategy due to their the nearest 0.1 g (Table 1). After ability to consume locally available food dissection, the fish digestive tract was items (Grabowska et al., 2009; Cerwenka removed and kept in 10% formaldehyde. et al., 2014). Their contents were identified to the In Iranian coastal waters of the Caspian lowest possible recognizable taxon and Sea, there are differences in some counted. Feeding strategy and prey important ecological factors including importance were given by modified substrate type, slope and light intensity graphical Costello method (Cortéz, 1997) (Aubrey et al., 1994; Khoshravan et al., with three dimensional representation of 2011) which may affect the prey percentage by frequency of occurrence community. Therefore, this study was (O%= ΣNi/ΣN) × 100), percentage by carried out to compare dietary composition number (N%= (ΣSi/ ΣSti) × 100) and of P. bathybius at three different localities percentage by weight of the various preys

(Bandar-e-Anzali, Salmanshahr and (W%= (ΣWi/ ΣWti) × 100), where Ni is the Miankaleh) along the southern Caspian number of predators with prey i in their Sea coastal waters. stomach, N is the total number of

predators with stomach contents, Si the Materials and methods stomach content (number) composed by

Fish samples were collected in April 2014 prey i, and Sti the total stomach content of from three localities located in Bandar-e- those predators with prey ‘i’ in their Anzali, Guilan Province (37º 28’ N, 49º stomachs. 27’ E), Salmanshahr, Mazandaran (36°42’N, 51°11’E) and Miankaleh, Mazandaran (36º 51’ N, 53º 34’ E) along the Iranian south coast of the Caspian Sea (Fig 1). A total of 290 specimens were collected using long beach seine during March and April 2014. Because of limit range of fishing months (from mid- September to mid-April) and cold weather conditions which had affected the deepwater goby migration toward the shallower waters (where the collections Figure 1: Sampling localities in the southern were made), we had to catch the Caspian Sea: Bandar-e-Anzali, Salmanshahr and Miankaleh. specimens only in March and April. All specimens which collected were males Iranian Journal of Fisheries Sciences 15(4) 2016 1618

Table 1: Number of specimens (N), total length graphical Costello method obtained from (TL) and weight (W) of Ponticola bathybius in sampling localities. three localities, feeding in deepwater goby is heterogeneous, with most predators locality N TL (mm) Weight (g) specializing in N. pallasi for Salmanshahr Bandar-e- 130 25.94±6.66 198.55±38.13 (IRI= 51.44%) and unrecognizable gobiid Anzali fish for Bandar-e-Anzali and Miankaleh Salmanshahr 80 24.50±1.62 169.31±45.99 localities (IRI= 55.71% and 53.41%,

Miankaleh 80 27.53±1.43 264.24±45.60 respectively) (Figs 2A, B and C). Feeding strategy of deepwater goby is much more Feeding intensity was analyzed by vacuity specialized diet in all localities, as a few index [VI= (number of empty predators often take large numbers of stomachs/number of stomachs examined) heavy food items. Cardium sp. in Bandar- × 100] (James, 1967). Index of relative e-Anzali and Clupeonella sp. and N. importance (IRI= (N%+W%) × O%) was malanostomum in Salmanshahr were calculated to determine the prey absent, while Cardium sp. was rare item in importance. This index has been expressed Salmanshahr. Whereas each food item had as: IRI%= (IRI/ΣIRI) × 100 (Pinkas et al., been consumed by only a few numbers of 1971). Shannon index which is described the predators with little or no overlap in by Krebs (1999) was computed to the resources used, there was a population determine the species diversity in the diet with a high between phenotype for all localities. Statistical processes and components (BPC) to the niche width in tests were performed using Excel v. 2007, each locality. This shows P. bathybius has SPSS v. 19 and Primer v. 6. a narrow dietary niche in all localities. However, the niche width was similar in Results and discussion three localities; the resource consumption Totally, six preys taxa were identified in patterns of P. bathybius had some the digestive tract of P. bathybius in all differences. So the Shannon index for localities: Neogobius melanostomus, N. Bandar-e-Anzali, Salmanshahr and pallasi, Clupeonella sp., Atherina boyeri, Miankaleh were obtained as 1.2, 0.7 and Cardium sp. and unrecognizable gobies 1.6, respectively. fish. According to the three dimensional

1619 Tajbakhsh et al., A study of food consumption of the deep water Goby Ponticola bathybius …

Figure 2: Feeding strategy of P. bathybius in sampling localities (A) Bandar-e-Anzali; (B) Salmanshahr and C) Miankaleh displayed with the Costello (1990) graphical method modified by Cortés (1997). Abbreviation denote: G, unrecognizable gobiid fish; M, Neogobius melanostomus; P, Neogobius palasi; Cl, Clupeonalla sp; A, Atherina boyeri; Ca, Cardium sp.. Iranian Journal of Fisheries Sciences 15(4) 2016 1620

Recalculation of O% and IRI% for probably, due to changes in the Gobiidae (including N. pallasi, N. macrobenthos community resulted from melanostomus and unrecognizable gobiid changes in the substrate type (Cerwenka et fish) as a higher taxonomic group yields al., 2014). values of >74% for O% and >72% for According to accomplished study on P. IRI%, respectively for all localities which bathybius, the fish forms the main resource indicates that the diet of the deepwater of it in coast of the Shikhovo-Karadagsky goby dominated by Gobiidae members region of the Caspian Sea (Miller, 2003). with large number and large proportion of In Salmanshahr, Kalantarian et al. (2013) the total weight of stomach contents. found that P. bathybius as a piscivorous According to vacuity index (VI), the feeds on arthropods, crustaceans and deepwater goby can be categorized as a mollusks, while larger specimens feed moderate feeders group in Salmanshahr mainly on gobies species especially on N. and Miankaleh localities to an edacious pallasi. Moghimi (2014) indicated that feeders groups (0≤VI<20) in Bandar-e- gobies fish especially N. pallasi is the Anzali during spawning season predominant prey item in Bandar-e-Anzali. (40≤VI<60). According to Ghelichi (1999), the Gobiidae is the most abundant family deepwater goby of Miankaleh prefers N. after Cyprinidae in the Caspian Sea and P. pallasi and Benthophilus stellatus, while bathybius considers as a native species items such as some fish species, Cardium with a high abundance in this family sp. and crustaceans were consumed (Abdoli and Naderi, 2009). Their occasionally. Jowshan (2012) found that abundance can be affected by the presence the fish such as gobies species, of prey and predator. Hence, awareness Clupeonella sp., Atherina boyeri, Rutillus about their food resources is important for sp. and Gasterosteus aculatus were taken predicting their impact on food change in up by larger specimens, while ecosystem (Abdoli et al., 2012). chironomidae, polychaeta (Nereis), The fish can shift their food preferences Cardium sp. and crustacean larvae were toward different dietary items during the consumed by smaller specimens. growth period. As the fish grow, they Our findings are in agreement with the usually shift from small and low mobility results of the above-mentioned prey items to larger and more motile items investigations, individuals fed (Opuszynski, 1979). In addition, some fish predominantly fish specially members of such as the Ponto-Caspian gobies have Gobiidae, but there are a few differences high plasticity to change their feeding in prey diversity. In this study, all patterns in new habitats (Grabowska et al., specimens were large and adult because of 2009). For example, the food preferences using beach seine with large mesh size (33 of Neogobius melanostomus and N. mm) and also sampling during spawning kessleri can be different in the upper season. For this reason, individuals Danube compared to their native habitat, specialized more on fish gain more energy. 1621 Tajbakhsh et al., A study of food consumption of the deep water Goby Ponticola bathybius …

This is notable that a lot of individuals be a more available food item comparing (43.78%) had empty gut because the males to other forage fishes. This study along are responsible for nesting and protecting with the other investigations approved that of the territory during the spawning period cannibalism occurs in deepwater goby (Miller, 1984). Temporal changes of prey especially in large size like some gobiid abundance (Kalantarian et al., 2013) species such as Knipowitschia panizzae affected by seasonal or annual changes are (Nonnis Marzano and Gandolfi, 2001) and one other reason to create these differences Ponticola kessler (Brandner et al., 2013). in the results. Also, this species shows some differences The slight differences observed among in food preference (mainly on fish) in localities can be also reflected in the comparison with other Ponto-Caspian features of habitat. Bandar-e-Anzali has a species of Gobiidae such as Neogobius fine to mid gravel bottom with a high gymnotrachelus, N. melanostomus and N. slope, Salmanshahr has a mid to rough pallasi feeding chiefly on invertebrates gravel bottom with high slope and (Grabowska and Grabowski, 2005; Abdoli Miankaleh has a muddy substrate with a et al., 2012). The larger size of deepwater gentle slope and in fact, decrease in the goby in comparison with the other goby sediment particles diameter is observed species of the Caspian Sea might possibly from west to east of south Caspian Sea due to its high energy intake. (Khoshravan et al., 2011). The type of substrate can lead to changes in References organisms’ community, as deposit feeders Abdoli, A. and Naderi, M., 2009. prefer the muddy substrate whereas the Biodiversity of fishes of the southern suspension feeders prefer to predominant basin of the Caspien Sea. Abzian on sandy bottom (Castro and Huber, Scientific Publication, 25, 785–786. 2008). On the other hand, light intensity Abdoli, A., Allahyari, S., Patimar, R. can also be effective in grazing and Kiabi B.H., 2012. Feeding invertebrate population by increasing algal strategies of three Neogobius species productions (Diggins et al., 2002). It in the Gomishan Wetland of Iran, seems that more preys are present in South-east Caspian Sea. Zoology in Miankaleh as a result of receiving more the Middle East, 56, 49–54. solar energy (light) in its gentle slope of Aubrey, D.G., Glushko, T.A. and muddy substrate and shallower water. Ivanov, V.A., 1994. North Caspian In this study, N. pallasi was dominant Basin: Environmental status and oil prey in all localities. This is in agreement and gas operational issues, Report for with the results obtained from Ghelichi Mobil-oil, 650P. (1999), Kalantarian et al. (2013) and Brandner, J., Auerswald, K., Cerwenka, Moghimi (2014). N. pallasi like its A.F., Schliewen, K. and Geist, J., predator P. bathybius is a benthic fish 2013. Comparative feeding ecology of (Tornaben et al., 2013). As a result, it can Iranian Journal of Fisheries Sciences 15(4) 2016 1622

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