ISSN 00329452, Journal of Ichthyology, 2014, Vol. 54, No. 8, pp. 584–590. © Pleiades Publishing, Ltd., 2014. Published in Russian in Voprosy Ikhtiologii, 2014, Vol. 54, No. 5, pp. 591–598.
Peculiarities of Embryonic Development of Round Goby Neogobius melanostomus (Gobiidae) in Fresh Water1 M. Bonis l awskaa, A. Tanskib, A. Brysiewiczc, A. KorzeleckaOrkiszb, W. Wawrzyniakd, and K. Formickib a Department
of Aquatic Sozology, West Pomeranian University of Technology, ul. Kazimierza Królewicza 4, Szczecin, PL71550 Poland b Department of Ichthyology, Hydrobiology and Biotechnology of Reproduction, West Pomeranian University of Technology, ul. Kazimierza Królewicza 4, Szczecin, PL71550 Poland c Institute of Technology and Natural Sciences, Western Pomeranian Research Centre in Szczecin, Szczecin, Poland d Department of Sustainable Development of Fisheries, Szczecin, Poland email:
[email protected] Received May 22, 2013
Abstract—The results obtained indicate the potential of the round goby to reproduce in fresh water, which may result in further expansion of the species to upper reaches of rivers and to other water bodies (lakes, dam reservoirs). Embryonic development of the round goby in fresh water proceeded in a regular manner. However, embryonic development in fresh water took a shorter time than in saline water. Although the newly hatched larvae were somewhat smaller than those hatching from eggs kept in saline water, the hatching rate was high (90%). If the species finds conditions suitable for reproduction in Polish freshwater bodies, it may pose a threat to numerous native freshwater fish species by taking over both their feeding and reproductive niches. DOI: 10.1134/S0032945214050026 Keywords: round goby, Neogobius melanostomus, invasive species, embryonic development, fresh water 1
INTRODUCTION Due to the strong expansion of its range worldwide, the round goby Neogobius melanostomus (Pallas, 1814)—originating from coastal waters of the Black, Caspian Seas, and Sea of Azov—is regarded as an invasive species (Charlebois et al., 1997; Charlebois et al., 2001, Corkum et al., 2004, Sapota and Skóra, 2005; Kornis et al., 2012). The main cause underlying the round goby’s (the species belongs to the family Gobiidae) appearance in numerous areas, both marine and freshwater, are nonintentional anthropo genic introductions. Ships’ ballast waters have been, and still are, transporting numerous species of aquatic organisms, including fish. Wonham et al. (2000) list as many as 32 alien fish species introduced to various areas via waterborne transport. In the Polish waters, the round goby appeared more than 20 years ago, most probably in 1987, in the port of Gdynia; the first specimen having been caught in June 1990 off the port in Hel (Skóra and Stolarski, 1993). The round goby occurs both in saline and fresh waters. As shown by numerous studies, the round goby enters numerous rivers, including the Danube, Volga, Ural, Sava, Samara, and Ontario R. in North America (Berg et al., 1949; Maclnnis and Corkum, 2000; Jura jda et al., 2005; Beek, 2006; Lusk et al., 2010; Raby
1 The article was translated by the authors.
et al., 2010; Piria et al., 2011; Shemonaev and Kiri lenko, 2011) as well as lakes, including those of North America where it has established large populations (Charlebois et al., 1997; Czapp et al., 2001; Marsden et al., 2007; Shemonaev and Kirilenko, 2009; Kornis et al., 2012). Environmental conditions of the Gulf of Gdañsk, favorable for the species, enhanced its spread to other coastal areas of the Baltic Sea, including the Pomeranian Bay (Skóra and Stolarski, 1995; Sapota, 2002). Due to the high plasticity of this species, in the late 1990s the round goby appeared in Polish freshwa ter reservoirs: in the lakes Lebsko and Gardno (Ciepielewski and HornatkiewiczZ· bik, 2003), Dabie (Biernaczyk et al., 2010), in the Vistula Lagoon (Borowski, 1999) and in the estuary of the river Odra (Czuga l a and Wozniczka, 2010). Since the time the species invaded Polish waters, it has been in the focus of attention of research carried out at the Marine Research Station of the Institute of Oceanography, University of Gdansk (Skóra and Stolarski, 1993, 1995; Sapota, 2004; Sapota and Skóra, 2005). Accord ing to Wandzel (2000), the round goby was caught in 34 tows effected, during 13 cruises in 1993–1999 in the Puck Bay as well as in the open sea (off Hel and Jast araia). The species’ population continues to expand. In 1996, the round goby accounted for, on the average, 0.16% of the total weight of fish caught in research
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catches in the Puck Bay, an almost 100fold increase (up to as much as 15.16%) being recorded in 1999 (Wandzel, 2000). It should be mentioned that the round goby, simi larly to the monkey goby Neogobius fluviatilis (Pallas, 1814), has commercial importance. Its meat used to be canned, the product being called “bychki v tomate” (Eng. gobies in tomato sauce), the Polish name being derived from a characteristic shape of the species’ head which makes up to 22–23% of the total body length (Berg et al., 1949). The round goby spawns from April until August, and even September (the Black, Caspian seas, and Sea of Azov), the fish laying 200–2700 eggs (Berg et al., 1949); 800–6177 eggs were reported by Nikolsky (1954), and 328–5221 eggs—by Kovtun (1978); the number of eggs in the North American lakes being recorded as 300–5000 (http://el.erdc.usace.army.mil/ ansrp/neogobius_melanostomus.pdf). Skóra and Sto larski (1995), and Sapota (2004), who studied the spe cies in the Gulf of Gdansk, described the spawning season as extending from April until July (Skóra and Stolarski, 1995), whereas Sapota (2004) found the spawning to be intensified between April and May and between July and September. The absolute fecundity of the round goby in the Gulf of Gdansk was found to range within 89–3824 eggs (mean 1739) (Wandzel, 2000) and 94–2190 (mean 645) (Tomczak and Sapota, 2006). The eggs are laid in portions, at the depth of 0.5– 3.0 m, occasionally down to 6 m, at the water temper ature of 10–12°С (eggs are laid in masses at 15–16°С) (Berg et al., 1949; Nikolsky, 1954), and even 26°C in the Caspian Sea (Kovtun, 1979). The male guarding the nest (usually a small burrow, an overturned shell, or a sunken object) becomes black in colour and takes care of the eggs until the last larva has hatched. The fertilized eggs, ellipsoid in shape (3.3–4.6 mm high and 1.5–2.1 mm wide) are being glued to the nest walls and/or ceiling and, as a rule, hang down; the male, by fanning its fins, aerates the water, which provides excellent oxygen conditions for the developing embryos (Berg et al., 1949, Miller, 2003; Samsel, 2006, Meunier et al., 2009). The newly hatched after 4–7 days at 19–20°C larvae are welldeveloped, their fins containing rays (Berg et al., 1949); the larvae attach themselves with ventral suckers to the nest. According to Moskal’kova (1978, 2007), the individu als leaving egg membranes are advanced in their devel opment so that they can be regarded as fry. Moiseyeva (1983) described the formation of primordial germ cells in the round goby during the embryonic develop ment; the newly hatched larvae, 5.8 mm long, had nondifferentiated gonads. The expansion of this new fish species, mainly in the coastal waters of the Baltic Sea, as well as its incur sion into fresh waters, poses numerous threats. The round goby is a dangerous species because, to ensure population persistence, it has developed a number of JOURNAL OF ICHTHYOLOGY
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adaptations, portion spawning, nest construction, brood care, a characteristic shape of eggs and their fast attachment to the substrate, short duration of embry onic development, adaptation of the newly hatched individuals, which resemble adults, to independent life (the absence of larval stage). In view of all those facts and information, an attempt was made to breed this species, alien in the Polish waters, in fresh water to find out to what extent the round goby is capable of invading inland waters. MATERIALS AND METHODS The study was carried out in June 2002 in the aquaria of the Department of Ecology and Protection of the Sea, Faculty of Natural Sciences, University of Szczecin and in the isothermal laboratory of the Department of Fish Anatomy and Embryology, Agri cultural University of Szczecin (at present: the West Pomeranian University of Technology in Szczecin). Adult individuals (7 males—average length—151.4 ± 2.3 mm and 5 females—124.3 ± 1.9 mm) were col lected from the Puck Bay (Fig. 1). The fishes were released to about 1000 dm3 tank with the bottom covered by sand, stones, and ceramic pipes. For the first 4 days, the fish were kept in saline water (brought from the Puck Bay–6.0PSU Practical Salinity Unit = 6.0‰). Subsequently, the water was diluted by adding fresh (tap) water until it became entirely fresh. The basic physical and chemical fresh water quality parameters were determined two times in the month (Table 1). Seven days after the release, the fishes spawned naturally. The newly laid eggs glued to different sub strates were carefully transferred to a tank filled with fresh water. The embryonic development of the round goby was observed and documented with the aid of a set of equipment consisting of a stereomicroscope (SMZ 1500) equipped with a microprocessor controls (Trol–8100/9100), a digital camera (Nikon DS. Fi–1), a Nikon monitor, a VCR, and a computer. Photographs of the eggs (n = 30) were taken after the completed swelling and at the stage of fully developed embryo, and were saved. Measurements of egg height and width as well as the yolk sphere diameter were taken from the saved images using the Multiscan v. 13.01 software. The yolk sphere diameter served to calculate the yolk volume (equation 1.1): V = 4/3πr3, (1.1) where r—yolk sphere semidiameter, mm. The software mentioned was used to measure the fol lowing dimensions of the newly hatched larvae (n = 30): the total body length (TL), yolk sac length (l), and yolk sac height (h); the yolk sac volume (Vs) was calculated using the formula for elongated ellipsoid (Blaxter and Hemple, 1963) (equation 1.2): Vs = 1/6πh2l. (1.2)
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Wladyslawowo BALTIC SEA
Jastarnia N
Puck Bay
Hel’
Fig. 1. Area from specimens of the round goby was collected. Jastarnia
The fry was grown out in 350 dm3 tanks filled with fresh water, sand and numerous hideouts being placed on the tank bottom. During the first month, the fry were fed frozen cyclopoids 3–4 times a day. Later on, the diet was gradually enriched by adding frozen (minced) krill and live chironomid larvae. The experi ment was terminated after 30 and 90 days. At the stage of resorbed yolk sac, the fry (30 individuals) were mea sured to 0.01 mm. On termination of the experiment, the fry—in addition to being measured—were also weighed to 0.01 g, using a WXD 200/2000 electronic scales.
Duration of the embryonic development is given in degreedays (DD°) (a product of the number of days it took to complete the embryonic development and mean daily temperature). The survival rate, expressed as a percentage of hatched larvae, was determined on termination of hatching in a group of selected fertil ized eggs from one female (about 50). Statistical treatment of the results (effected with the Statistica 9.0 PL software) involved Duncan’s multiple range test applied to compare mean values of egg parameters (egg height and width, yolk sphere
Table 1. Selected physical and chemical fresh water parameters during the experiment Water quality parameter Temperature, °C Salinity, PSU Dissolved oxygen content, mg O2 dm–3 pH Alkalinity, mg CaCO3 dm–3 Hardness, mg CaCO3 dm–3
Value 20.0–21.0 0.4–0.5 7.0–8.5 7.5–8.5 130.1–180.1 325.3–475.4
Standard analysis Elmetron CX–701 Elmetron CC–103 Standard Methods…, 2005 Elmetron CX701 Standard Methods …, 2005 The same
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Table 2. Dimensions of round goby eggs from one female, (n = 30; mean values ± SD) Stage of embryonic development
Egg parameter Egg height, mm Egg width, mm Yolk sphere diameter, mm Yolk sphere volume, mm3
fine morula
devoloped embryo
2.79 ± 0.48 1.78–3.69 1.95 ± 0.15 1.74–2.59 1.95 ± 0.15 1.74–2.01 3.44 ± 0.36 2.76–4.24
2.76 ± 0.20 2.48–3.18 1.35 ± 0.04* 1.27–1.40 1.13 ± 0.06* 1.04–1.26 0.77 ± 0.13* 0.59–1.06
* Means denoted with identical indices are not significantly different, p > 0.05; Duncan’s multiple range test.
diameter and volume) at selected stages of the embry onic development. RESULTS Egg characteristics. The fertilized round goby eggs were very peculiar in shape: initially in the embryonic development, they were pearshaped to become more ellipsoid later on. The rounded end features a tuft of filaments used to attach the egg to nest walls. The round goby eggs examined were observed to differ in their size parameters (height and width) at selected stages of the embryonic development (Table 2). Both at the small blastomere morula stage and later in embryonic development, the mean egg heights were similar (no significant differences). As the embryonic development progressed, the egg width and the size of the yolk spheres (diameter, volume) were observed to decrease (Table 2), which is related to the embryo development and growth within the egg. Embryological development: a brief outline. Egg swelling, i.e., the formation of the perivitelline space, took about 45 min at 20.0°C and ectoplasm colleted on the animal pole. Cleavage—the first cleft appeared 60 min after fertilization (0.8 DD°) and sixteen blas tomeres are visible at 1.8 DD. The stage late morula appeared at 3.4 DD° (Fig. 2). Gastrulation commenced after 3.8 DD° and ended after about 15.0 DD° and the blastopore closed off. Where was embryo with emerg ing cephalic part and distinct 4 myomeres. An outline of the embryo was visible in the egg after 24 hours (20.0 DD°) when the formation of eye cups and primary brain vesicles. At 70 DD, eye lenses were visible, the heart began pumping the colourless blood, while strong pigmentation of the eyes could have been observed 7 days after fertilization (140 DD°) (Fig. 3). Hatching began the next day (about 160 DD°) and took about 1.5 days (Fig. 4). The newly hatched larvae measured, on the aver age, 5.00 ± 0.32 mm; the yolk sac mean length and height were l = 1.32 ± 0.10 mm and h = 1.07 ± 0.16 mm, JOURNAL OF ICHTHYOLOGY
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respectively, resulting in mean volume of 0.81 ± 0.22 mm3. The larval survival rate in the experiment was 90%. Fry growout. Five days after hatching, when the yolk sac was resorbed in twothirds, the fry began active feeding on frozen cyclopoids. The yolk sac was completely resorbed 7 days after hatching, when the larval length averaged 10.36 ± 0.76 mm (min 8.51; max 11.42 mm). At that time, the fish body (head, trunk) showed the presence of strong pigmentation and the fry began active swimming in the water; occasionally, the fish attached themselves to the substrate. At that time, the mortality rate was very low (about 1%). Thirty days after hatching, the fry began to feed on minced krill and live chironomid larvae. There were large size differences between the fry, the differences increasing with time. The experiment was terminated after 90 days, resulting in the fry measuring (total length) from 16.25 to 32.00 mm (mean length 24.81 ± 5.40 mm) and weighing from 0.03 to 0.41 g (mean weight 0.18 ± 0.11 g), and fully resembling adults (Fig. 5).
1 mm Fig. 2. A round goby egg at the terminal stage of gastrula tion.
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1 mm Fig. 3. Embryos shortly before hatching (140 DD°).
DISCUSSION The round goby, an alien species, has seamlessly adapted to both brackish (Baltic) and fresh waters (riv ers, lakes) of Poland. As shown by the data discussed above, the conditions prevailing in certain parts of the Gulf of Gdansk are suitable for the species, rendering the Gulf an excellent spawning ground. The species is known for its high environmental tolerance. Salinity differences and low oxygen concentrations (e.g., 0.3– 0.9 mL dm–3—the fish is capable of breathing through the skin in 13%) are not barriers for dispersal of the species which is also capable of living in polluted water (http://el.erdc.usace.army.mil/ansrp/neogobius_mela nostomus.pdf). As shown by the data obtained in the experiment, despite certain differences during embryonic develop ment which proceeded in fresh water, the process itself was regular and was terminated by the emergence of healthy hatchlings. The differences concerned the egg size. In this study, the egg height was 1.78–3.70 mm (Table 2), i.e., was by about 1.0–1.5 mm lower than that reported by Berg et al. (1949) (3.3–4.6 mm) and Moskal’kova (1989) (3.4–3.8 mm). The duration of embryonic development in fresh water (8 days) was by 2–3 days longer than the duration reported by Berg et al. (1949), by 7–8 days shorter than that reported by Moiseyeva (1983), and by 4–5 days shorter that that reported by Kozik (1999). It may be presumed that the discrepancies were caused by differences in water salinity and temperature. In the Sea of Azov, the round goby spawns at 15–16°С and optimal salinity of 9.5– 11.0 PSU (Smirnov, 1986), whereas Kozik (1999) bred the species at water of different salinities (2.0, 7.0, and 12.0 PSU) and at 20.0°C. Obviously, increased water temperature during embryogenesis results in short ened duration of the embryonic development and in reduced size of the newly hatched larvae.
1 mm Fig. 4. A hatching larva.
The freshwater effect on embryonic development of the round goby is manifested not only as the smaller egg height and shorter duration of embryogenesis, observed in this study, but also as the size of the larvae and their developmental advancement. As observed by Moiseyeva (1983), the larvae hatching after 18 days of embryonic development in sea water were by 0.5–0.8 mm longer than the hatchlings obtained in this study. This is a regularity mentioned by MacInnis and Corkum (2000): the round goby individuals aged 1, 2, and 3 years from sea water were longer than those caught in brack ish and freshwater areas. Despite those differences in larval size and duration of embryonic development, the survival rate of the embryos was very high (90%), similar to that obtained
Fig. 5. The round goby fry 90 days after hatching. JOURNAL OF ICHTHYOLOGY
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REFERENCES Beek, G.C.W., The round goby Neogobius melanostomus first recorded in the Netherlands, Aquat. Invasions, 2006, vol. 1, pp. 42–43. Berg, A.S., Bogdanov, A.S., Kozhik, N.I., and Rass, T.S., Promyslovye ryby SSSR (Commercial Fish Species in USSR), Moscow: Pishchpromizdat, 1949. Biernaczyk, M., Opanowski, A., Neja, Z., and Stepanowska, K., The emergence of invasive species – round goby Neogobius melanostomus (Pallas, 1811) in D a¸bie Lake, in Proc. Natl. Conf. “Natural and Anthropological Transformation of Lakes,” SzczecinStare Drawsko, 2010, p. 10. Blaxter, J.H.S. and Hemple, G., The influence of egg size on herring larvae (Clupea harengus), J. Cons. Int. Explor. Mer., 1963, no. 28, pp. 211–240. Bonis l awska, M., Effects of salinity on the duration and course of embryogenesis in sea trout (Salma trutta L.), J. Pol. Agric. Univ., 2009, vol. 12, no. 4. http://www.ejpan. media.pl/volume12/issue4/art07.html Bonis l awska, M., KorzeleskaOrkisz, A., Winniski, A., Formicki, K., and Szaniawska, D., Morphophysiological aspects of the embryonic development of ruffe Cymnoceph alus cernuus (L.) under different thermal conditions, Acta Ichthyol. Piscator., 2004, vol. 34 (1), pp. 51–74. Borowski, W., Round goby in Vistula Lagoon, Mag. Fish Ind., 1999, vol. 4, no. 12, pp. 39. Charlebois, P.M., Marsden, J.E., Goettel, R., et al., The round goby Neogobius melanostomus (Pallas): a review of European and North American literature, Ill. Nat. Hist. Surv., Spec. Publ., 1997, no. 20. Charlebois, P.M., Corkum, L.D., Jude, D.J., and Knight, C., The round goby (Neogobius melanostomus) invasion: cur rent research and future needs, J. Great Lakes Res., 2001, vol. 27, no. 3, pp. 263–266. Ciepielewski, W. and HornatkiewiczZ· bik, A., The diver sity of ichthyofauna in Lakes S l owinski National Park, Kom. Rybackie, 2003, vol. 2, pp. 22–26. Corkum, L.D., Sapota, M.R., and Skóra, K.E., The round goby Neogobius melanostomus, a fish invader on both sides of the Atlantic Ocean, Biol. Invasions, 2004, vol. 6, pp. 173–181. Czapp, D.F., Schneeberger, P.J., Jude, D., et al., Monito ring round goby (Neogobius melanostomus) population expansion in eastern and northern Lake Michigan, J. Great Lakes Res., 2001, vol. 27, pp. 335–341. Czuga l a, A. and Wozniczka, A., The river Odra estuary— another Baltic Sea area colonized by the round goby Neogo bius melanostomus Pallas, 1811, Aquat. Invasions, 2010, vol. 5, pp. 61–65. Jakubas, D. and Mioduszewska, A., Diet composition and food consumption of the grey heron (Ardea cinerea) from breeding colonies in northern Poland, Eur. J. Wildl. Res., 2005, vol. 51, pp. 191–198. Jurajda, P., C erny, J., Pola cik, M., et al., The recent distri bution and abundance of nonnative Neogobius fishes in the
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viving under unfavorable conditions created by pol luted, poorly oxygenated ships’ ballast waters. In addi tion, industrial pollution resulting in increased salinity of Polish rivers may contribute to the creation of con ditions enhancing reproduction of the round goby.
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by Kozik (1999) in sea water, which may indicate that the species, alien in the Polish waters, is capable of reproducing in fresh water, should other environmen tal conditions (particularly the substrate amenable to nest building) be favorable. As shown by the review of the relevant literature and by the results of this study, the newly hatched round gobies resemble adults and are well adapted to live independently, for which rea son the mortality rate during fry growout was very low. In her longterm studies, Moskal’kova (2007) found the yolk sac, the embryo’s energy supply, to have been very intensively resorbed during embryonic develop ment, the process being shown by histochemical anal yses to be associated with the presence of specific “cir culation system” responsible for food supply to the intestinal cavity. She suggested the system to be similar to that present in embryos of higher vertebrates, e.g., the sheep or the pig. According to Moskal’kova (2007), the egg membranes and the perivitelline space are analogous to the amniotic sac and amniotic cavity of higher vertebrates. Our study did not show such a rapid yolk sac resorption in those individuals hatched from eggs incubated in fresh water, which could have been caused by, on the one hand, egg incubation temperature and, on the other, the content of minerals in the water. The large size variability observed in the round goby fry grown out in fresh water could have been an effect of the high variability in egg size, as observed earlier (Table 2). The appearance of the round goby, classified among the Nonindigenous Estuarine and Marine Organisms (NEMO), results in serious disturbances in native ecosystems and affects their biodiversity. Research carried out in the Puck Bay demonstrated the round goby to out compete the native gobiids (the black goby, Gobius niger Linnaeus, 1758, the common goby, Pomatoschistus microps (Krøyer, 1838), and the sand goby, P. minutus (Pallas, 1770) by occupying their spawning sites (shelters) and by having a diet similar to that of the native gobies (Skóra and Rzeznik, 2001; Karlson et al., 2006). The study carried out in 2006– 2007 showed the round goby present in certain areas of the Gulf of Gdansk to be characterized by increasing body length; more importantly, the fish lives for up to 5 years (4 years being the life span in the PontoCas pian seas) (Soko l owska and Fey, 2011). The enlarged round goby population in the Gulf of Gdansk was also observed to be related to increased populations of cor morants and herons feeding on it (Jakubas and Mio duszewska, 2005). Presumably, this has altered the food chain typical of the local ecosystem. The research and observations carried out so far show the species to be well adapted, already during early ontogenesis, to developing under very variable environmental conditions, as evidenced by the high survival rate of the larvae and low mortality among the grownout fry. This augments the hazard posed by the species, capable of penetrating both marine and fresh waters, be it clean or polluted. The eggs can be easily transported (they have filaments with which they are fast attached to the substrate) and are capable of sur
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2014