Is the body condition of the three-spined stickleback (Gasterosteus aculeatus) determined by the type of food consumed?

Gasterosteus aculeatus is a small fish widely distributed in the northern hemisphere (Wootton 1984). In the Gulf of Gdańsk, it occurs mostly in the inshore shallow waters (Skóra et al. 1992; Sapota & Skóra 1996; Lizińska 2002; Waligóra Borek et al. 2006). This region is also an important feeding and spawning area for many commercial fish species (Skóra 1993). The research on prey of the three-spined stickleback has been carried out by many authors but the results are ambiguous. Manzer (1976), Hosted et al. (1988) and Peltonen et al. (2004) noticed that the sticklebacks prey mainly on plankton, while Thorman & Wiederholm (1986) found mostly benthic organisms in fish stomachs. Other authors observed both planktonic and benthic organisms (Dukowska et al. 2009; Thorman & Wiederholm 1983; Jakobsen et al. 1988; Kislaioglu & Gibson 1977; Wootton 1976). Wootton (1976) reported that G. aculeatus eats plankton in summer, while benthic organisms and plants in winter. The stickleback also feeds on spawn and fry of commercial fish (Kotterba et al. 2014; Nikolsky 1956). This may result in the displacement of fry of these species from the shallow water zone and the reduction of their populations (Kotterba et al. 2014; Skóra et al. 1992).

The study from Puck Bay shows that the three-spined stickleback has a wide range of nourishment components and preys on both plankton and benthic organisms (Skóra et al. 1992).

The aim of this study was to compare the body condition of G. aculeatus caught in three regions of the western part of the Gulf of Gdańsk (Hel, Chałupy and Sopot), which differ in terms of environmental characteristics and a potential food base of the fish. Due to its high abundance, the species may affect the reproduction and the growth of other fish by feeding on their fry and larvae. The population growth observed in the Baltic Sea may be a cause for concern especially due to the decline in the catches of some important fish species.

The study of diets and food habitats of fish and other marine vertebrates through the examination of stomach contents is still a standard practice (Hyslop 1980; Cortéz 1997; Brush et al. 2012). The most commonly used measurements (numerical abundance, frequency of occurrence and volume or weight) provide different types of information on feeding habits (Macdonald & Green 1983; Bigg & Perez 1985; Cortés 1997; Cortés 1998). This information combined with the body condition index could partly reflect the exploitation of the available food resources (Cortés 1998).

In the 1980s and the 1990s, G. aculeatus was the most abundant species in the shallow coastal area of the Gulf of Gdańsk (Lizińska 2002; Sapota & Skóra 1996; Skóra et al. 1992; Skóra 1993). The occurrence of Neogobius melanostomus in the Baltic ecosystem changed the fish community structure. Since 2004, we have observed the dominance of two species, i.e. round goby and stickleback, in the shallow water (Sapota 2004; Sapota & Skóra 2005). The number of round goby nests in this area is very high (Sapota et al. 2014).

Consequently, a question arises whether the stickleback grazes on round goby eggs, thereby reducing the rate of invasion?

During the conducted research, individuals of G. aculeatus were caught in the shallow water zone of the Gulf of Gdańsk. It was a dominant or co-dominant species in all samples.

The sampling region is characterized by the variability in environmental conditions and heterogeneous bottom (sand, stones, vegetation). Specific conditions in the eulittoral zone affect the quality, composition and quantity of a potential food base (Kotwicki 1997; Elliott et al. 2002) and this determines the fish feeding strategy (Morawski 1978; Costa et al. 2002). The majority of energy-cost processes (intensive growth, spawning) of sticklebacks occur in spring and summer (Wootton 1984) and according to Wootton (1994), the metabolic demands increase with temperature.

Stickleback is a well-known omnivorous opportunistic feeder (Wootton 1984). It feeds on various animals depending on the biocenosis structure and environmental conditions. Quantitatively the most important food components in three-spined stickleback guts were Crustacea – planktonic (Calanoida, Cladocera) and benthic Harpacticoida. According to Peltonen (2004), sticklebacks prey mostly on planktonic crustaceans. Copepoda eggs, which quantitatively dominated in spring samplings most likely get into the fish guts together with the consumed females. Benthic components were represented by Batyporeia sp., Nematoda and Gonothyrea sp. According to the study conducted in the Archipelago of SW Finland, Corophim volutator, Hediste diversicolor, Gammarus sp., Chironomids and plankton were the most important prey (Rajasilta 1980). Based on the analysis of the stickleback diet, the potential competition for food between stickleback and young round gobies can be excluded. According to Rzeźnik and Skóra (2001), young round goby (20-40 mm) in the Gulf of Gdańsk feed mostly on Polycheta and Crustacea.

Fish eggs were found in the guts of fish from all samples. It is possible that herring eggs were present in the Sopot area in spring. According to Kotterba et al. (2014), the three-spined stickleback is considered to be the most important piscine herring-spawn predator within the Baltic Sea lagoons and estuaries, and the Sopot sampling site is located near the potential herring spawning area (BRISK 2010).

Fish eggs were present in large quantities in the stomachs of fish collected during summer in Hel. They were probably stickleback eggs coming from damaged nests. Hynes (1950) reported that it is a common situation that males eat eggs from their nests and non-breeding males and females raid the eggs from nests.

Parts of the imago of insects found in the samples from all the locations were an interesting finding. Large quantities of insect remains in the fish stomachs may prove intentional selection of this dietary component. Insects probably accidentally fell into the water or were feeding on algae decomposing on the shore and were washed away by waves. It is known that stickleback can feed near water surface (Peltonen et al. 2004). In the literature, we found only a short report about the remains of insects in the stomachs of sticklebacks in the publication by Hynes (1950) – the author referred to the research by Blegvard (1917) on the diet of stickleback – and a short note about insects found in the diet of stickleback from Estonia (Saat & Turovski 2003). Taking into account our data, it would be useful to analyze the significance of insects in the diet of sticklebacks from the shallow coastal seawaters.

The feeding patterns are influenced by environmental, behavioral and physiological factors (Cortés 1997). The research was carried out during warm months, which excludes a negative effect of biotic (lack of food) or abiotic factors (temperature changes) affecting the feeding (Thorman & Wiederholm 1983; Złoch et al. 2005). The observed differences in the stomach fullness index must due to other factors. It should be kept in mind that feeding is also related to the fish size (Grodziński 1971; Herczeg et al. 2013), because the diet composition changes during the ontogenesis of fish (Złoch et al. 2005). It can be noticed that smaller fish feed more intensively than the larger ones, probably due to their faster growth rate (Grodziński 1971; Kapoor & Bhavna Khanna 2004; Wootton 1984, 1994). At the early stage of development, fish need to cover the cost of a higher metabolic rate, with becomes slower in the case of adult fish (Nikolski 1963). The highest stomach fullness index was determined in Chałupy, probably because the smallest fish were caught there in large quantities (Fig. 2, Fig. 4). The smallest value of the index value was determined in Sopot in summer due to the presence of the largest fish (Fig. 2, Fig. 4).

The stickleback stomach analysis has shown that planktonic prey includes both Cladocerans and Copepods (Peltonen et al. 2004). In the presented work, the food selectivity index was calculated for three food items (Cladocera, Copepoda, Nematoda), because data on the quantity of other items in the environment were not available or they were defined as absent. Ivlev’s indices shows that the three-spine stickleback was avoiding Copepoda at the Hel sampling location in spring and summer, while choosing Cladocera in both seasons. According to Peltonen et al. (2004), three-spined sticklebacks in the Gulf of Finland (the East Baltic) feed mostly on zooplankton. It is known that periodical accessibility of the easily available food categories changes the food preferences (Dukowska et al. 2009). The research of Lefebure et al. (2014) shows an increase in G. aculeatus attack rates with temperature, and Persson (1987) concludes that this fish has generally a higher attack rate in the case of slow moving cladocerans compared to the fast moving copepods. This may suggests that fish select from the available food types those prey that provide the highest net energy gain (Stephens & Krebs 1986).

Fulton’s body condition was treated as an index reflecting the use of environmental resources.

The body condition index was calculated separately for all individuals caught at all three sampling locations. There were no significant differences in the index values (Fig. 5). According to ANOVA analysis, the G. aculeatus body condition in spring and summer was independent from the season and dependent on the total fish length and sampling location.

During the spring research on benthos and plankton structure in Sopot (data from the COSA project), macrobenthos was dominated by Crustacea (Bathyporeia sp.), meiofauna by Nematoda and zooplankton by Rotatoria. Some of these taxa (Rotatoria) were not found in the stomach of three-spined sticklebacks from this region. A similar situation was also observed at other sampling sites – the organisms dominant in the environment were not always the most abundant food items in the fish stomachs. This means that not all the dominant organisms in the environment are eaten by the three-spined stickleback. This may suggest that G. aculeatus does not choose the dominant organisms but easy-to-catch or energy efficient prey. Stephens & Krebs (1986) suggested that the handling time (the amount of time spent by a predator to search and catch the prey) is balanced by the energy gained from eating the prey. Gill & Hart (1994) concluded that the decision whether to consume the prey depends on the relations between the size of prey, the size of predatory fish and the stomach fullness. This could be an explanation for the absence of some taxa in the fish stomach, while found in the environment.

It is also known that the composition of fish food may change during the day (Złoch et al. 2005) and seasons. The examined fish specimens were caught mostly during the morning samplings in warm months of the year, while the research carried out for 24 hours throughout the year could give us a different perspective on the food composition of the three-spined stickleback. Due to the annual changes in the food base as well as seasonal and daily changes in the metabolic rate of stickleback, we can expect differences in the food composition and quantity.

Despite the time of the study (2005), current random analyses of the stickleback gut content in similar locations show no significant differences in the prey of sticklebacks. The described feeding patterns are still observed.

The results of the research show that the three-spined stickleback can effectively prey on various food items, in various habitats of the Gulf of Gdańsk. Its body condition remains stable. No statistically significant differences in the fish body condition were found irrespective of the stomach content and the local food base in the study area.

All food items found in the fish stomachs were characteristic of the shallow water zone. The comparison of Fulton’s body condition index, the stomach content and the food selectivity index values in relation to environmental conditions reveals that the three-spined stickleback may effectively use the available food resources in spring and summer, regardless of their local composition.

Although there is no evidence that the stickleback can reduce the invasion of round goby by preying on its eggs, it is an important predator of eggs of other fish species in the shallow water zone.