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Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

Life history traits of an invasive population of bighead goby Neogobius kesslerei (Günther, 1861) from the middle Danube, including absolute and relative fecundity, egg size, number of spawning batches and size at first maturation, were examined and evaluated within an epigenetic context. Ripe bighead goby females attained 42.8–142.5 mm LS, with absolute fecundities ranging from 669 to 5646 eggs (mean 2109 eggs), and relative fecundities of 61.6–174.0 eggs g−1 body weight (mean 119.6 eggs). Egg diameters varied between 0.04 mm and 1.70 mm (mean = 0.57 mm). In the pre-spawning period there was no clear size distinction in eggs (0.12–1.45 mm; mean = 0.52 mm) in 34.1% of females; whereas in 65.9% of females, two egg size groups were distinguished: group I diameters of 0.06–0.85 mm (mean = 0.43 mm), and group II diameters of 0.55–1.70 mm (mean = 1.17 mm). Females with size-group II eggs at the beginning of the reproductive season were assumed to be ready to spawn and the others to be subsequent spawners. Bighead goby appears to be altricial compared to the round goby, although in both species a shift from highly precocial towards a less precocial life history was observed. These differences, affected by epigenetic mechanisms and resulting in alternative ontogenies, may have important implications for a species’ potential success in novel environments, favouring the round goby over short time periods (several years) and bighead goby over longer periods of time (decades and longer).


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

Successful invaders are generally believed to share some common features that enhance their chances of successful establishment in novel environments. One of these appears to be their phenotypic plasticity and/or biological flexibility (e.g. Balážová-Ľavrinčíková and Kováč, 2007; Fox et al., 2007; Tomeček et al., 2007), which is linked to changes in their environment (Ross, 1991; Hoffmeister et al., 2005). Consequently, biological invasions can result in both genetic and non-genetic changes in the invader; for example, shifts in gene expression, resource allocation (i.e. changes in life-history traits), morphology and physiology within the lifespan of an individual (Strayer et al., 2006).

The phenotypic plasticity of a species is associated with epigenetic mechanisms, which are usually expressed through the creation of both altricial and precocial forms within and/or among populations (Balon, 1990, 2004). These forms can be evaluated by a thorough examination of their ontogenies, especially early development, associated with studies of growth (e.g. Copp et al., 2004) and life history traits such as fecundity, age at maturity (e.g. Fox et al., 2007), number of spawning acts per season, parental care, egg size, age at maturation, as well as both among- and within-population ontogenetic variability in external morphology (Kováč and Siryová, 2005; Ľavrinčíková et al., 2005; Balážová-Ľavrinčíková and Kováč, 2007).

The bighead goby Neogobius kessleri (Günther, 1861) is a Ponto–Caspian gobiid species that originally inhabited the brackish zone on northern and western shores of the Black Sea, and lower parts of rivers entering the sea between the rivers Danube and Dnepr (Svetovidov, 1964). The history of the bighead goby’s invasion of the middle Danube begins back in the early 1990s (Zweimuller et al., 1996; Ahnelt et al., 1998; Pintér, 1998; Copp et al., 2005). However, bighead goby is not the only highly-invasive gobiid present in the middle and upper stretches of the Danube. In the past two decades, four non-native species of the genus Neogobius have been recorded in this area: bighead goby, racer goby Neogobius gymnotrachelus (Kessler, 1857), monkey goby Neogobius fluviatilis (Pallas, 1814), and round goby Neogobius melanostomus (Pallas, 1814). All of these species have been reported to spread rapidly (Copp et al., 2005), although racer goby and monkey goby appear to be rather limited in their density and distribution, respectively. Bighead goby, the first Ponto–Caspian gobiid invader of the middle Danube and previously the most abundant and widely distributed of the invading gobiids, has been recently outnumbered in both abundance and distribution dynamics by a subsequent invader, the round goby (Copp et al., 2005; Jurajda et al., 2005; personal observations, August 2007). The high frequency and abundance of these two species raise the question of their impact on the native fish community and ecosystem. Therefore, besides the study of life history traits of bighead goby that invaded the Danube, this paper also focuses on the life history traits of invasive round goby from the same sites. The aim was to analyse some life history trait differences between bighead and round gobies, and evaluate these together with our previous data on their morphology and ontogeny, within the epigenetic context. Finally, based on this evaluation, a reflection on possible further development in population dynamics of the two species is also made.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

In total, 236 specimens of bighead goby were collected by electrofishing from the River Danube at Čunovo (river 1851 km) and its Karloveské side arm (river 1873 km), Bratislava, Slovakia, between April and November 2004. The sample contained 70 females with developed gonads, 34 of which were collected during the pre-spawning period (1–29 April), 20 during the spawning period (7 May–21 August), and 16 in the post-spawning period (13 September–22 November). The samples were preserved in 4% formaldehyde. Standard length (LS) was measured using digital photographs taken with a Nikon CoolPix 5000 camera and the impor 2.31e software. Weight, eviscerated weight and gonad weight were taken to the nearest 1 mg, using the RADWAG balance WPS 360/C/2. Both absolute and relative fecundity (number of eggs per 1 g of eviscerated body weight) were evaluated in the specimens from the pre-spawning period only, whereas egg diameters and egg size groups were evaluated for all captured females. Fecundity was determined gravimetrically (Holčík and Hensel, 1972). For egg diameter analysis, 50 randomly-chosen oocytes were measured to the nearest 0.0025 mm using an ocular micrometer; egg size groups were then determined from the scatterplots of egg diameter distributions (Fig. 1). Spearman’s rank correlation test was used to test for correlations between absolute fecundity and LS, body weight and eviscerated body weight, between ovary weight and LS, and between the diameter of ripe eggs and LS. Subsequently, the best correlation fit was evaluated using F-tests.

image

Figure 1.  Example of egg size distribution in female bighead goby (LS = 70.5 mm; 50 eggs examined), River Danube (Slovakia), 14 April 2004. Note the gap between size group II (≥1.25 mm diameter) and eggs of subsequent prospective batches (size group I). The same pattern of egg size distribution was observed in round goby females (Fig. 1 in Ľavrinčíková and Kováč, 2007).

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The females of round goby, in both the pre-spawning (April; n = 55) and spawning period (May–November; n = 54), were collected in 2004 and 2005 from the same sites as those of bighead goby (see above). All methods of examination of their life history traits were identical to those used in the bighead goby (Ľavrinčíková and Kováč, 2007).

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

Bighead goby (all sexes) LS ranged from 24.5 to 148.6 mm (mean = 76.7 mm), with ripe females (n = 70) attaining 42.8–142.5 mm LS and body weights of 2.21–56.62 g (mean = 20.92 g). Absolute fecundity ranged from 669 to 5646 eggs and was significantly correlated with LS (P < 0.001, Fig. 2), body weight (P < 0.001) and eviscerated body weight (P < 0.001, Fig. 2). Mean absolute fecundity was 2109 eggs; mean relative fecundity was 119.6 eggs g−1 body weight, ranging from 61.6 to 174.0 eggs.

image

Figure 2.  Relationship between absolute fecundity and eviscerated body weight (top) and between absolute fecundity and standard length (bottom) of bighead goby (n = 34) from the Slovak stretch of the River Danube (Slovakia).

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Egg diameter varied between 0.04 and 1.70 mm (mean = 0.57 mm). However, in the pre-spawning period, two groups of eggs (Fig. 1) were clearly distinguishable in 65.9% females (Fig. 3). Diameters of egg size-group I ranged from 0.06 to 0.85 mm (mean = 0.43 mm), whereas those of egg size-group II ranged from 0.55 to 1.70 mm (mean = 1.17 mm) in diameter. Ovaries in the remaining 34.1% females contained eggs with no clear size distinction, ranging from 0.12 to 1.45 mm (mean = 0.52 mm). Females with size-group II eggs were assumed to be ready to spawn, i.e. at the beginning of the reproductive season, whereas the remaining females were assumed to be subsequent spawners. The mean diameter of ripe eggs did not increase significantly with body length (r2 = 0.02, P > 0.05). During the pre-spawning period, female gonad weight ranged from 0.078 to 5.424 g (mean = 1.520 g), and increased significantly with LS (r2 = 0.659, P < 0.001).

image

Figure 3.  Frequency distribution of egg diameters in bighead goby (top) and round goby (bottom) females from the River Danube (Slovakia) during the pre-spawning period.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

The phenotypic plasticity of a species, and often also the overall biological flexibility, depends on epigenetic mechanisms (Pérez et al., 2006). As a result, the life history of each population and/or species can vary back and forth, from generation to generation, along a trajectory between the most atricial (least specialised) and the most precocial (specialised) extremes (Balon, 2004). For the purposes of the present study, the evaluation of these forms consists of two steps: (i) native and non-native populations of bighead goby and round goby are compared, respectively, and (ii) bighead goby and round goby are compared to each other.

Native vs non-native populations of bighead and round goby

Shifts in life-history traits of invading bighead goby can be observed in the Slovak stretch of the Danube. Firstly, females reach reproductive maturity at a much smaller size (42.8 mm LS) than those of native populations (84–90 mm LS) in the Dnepr–Bug liman (Georgiev, 1966 c.f. Kalinina, 1976; Smirnov, 1986). Secondly, the absolute fecundity of the non-native Danubian population is conspicuously higher (669–5646 eggs: this study; 941–6664 eggs: Stráňai, 1999) than that of native populations (150–1500 eggs, Azov Sea: Kalinina, 1976). Moreover, bighead goby invading the middle Danube are spawning more than once per season, in contrasts to the single-batch spawning of native bighead goby (Kalinina, 1976).

Thus, although data on bighead goby in their native range are scarce, the higher absolute fecundity and shorter length at maturation of females from the Slovak Danube suggest that, on the altricial-precocial scale, the invading bighead gobies of the Danube have shifted altricially compared to the species’ native populations. A similar, though not as strong, pattern has been observed in female round gobies invading the Danube (Ľavrinčíková and Kováč, 2007), which were observed as achieving reproductive maturity at least 10 mm LS shorter (45.1 mm LS) than most of the native populations (Black and Azov seas), where female maturation has been reported to occur between 55 and 80 mm LS (Berg, 1949; Trifonov, 1955). Earlier maturity was also observed in round gobies invading the Slovak Danube, with 54.2% of females achieving reproductive maturity at age 1+ (M. Balážová et al., unpublished data). A similar pattern of early maturity at a small size has been reported for the species in its introduced North American range (MacInnis and Corkum, 2000; Balážová-Ľavrinčíková and Kováč, 2007). This contrasts round goby in their native range, where only 11% of fish age 1 and 60% of fish age 2 in the Dneprovsko–Bugski liman were mature (Pavlov, P. I., 1964: Current status of resources of industry fishes in lower Dnepr and Dneprovsko–Bugskoy liman and their conservation, Unpublished manuscript deposited in VINITI, in Russian). Similarly, in the middle part of the Caspian Sea, only 3% of round goby were mature at age 1+ and 60% at 2+ (Azizova, 1962). On the other hand, no significant differences in absolute fecundity and egg size were found between non-native and native round gobies (Ľavrinčíková and Kováč, 2007); therefore, the shift from the highly precocial life history of native round goby back towards a more altricial life history in its invasive populations does not seem to be as intensive as the shift found in bighead goby.

Bighead goby vs round goby in their introduced range

Analysis of the size-frequency distribution of eggs has revealed that non-native populations of both bighead and round gobies undergo asynchronic egg maturation, with multiple batch spawning of at least two batches (Stráňai, 1999; Ľavrinčíková and Kováč, 2007; this study). Comparisons of reproduction in nest-guarding batch spawners can be difficult (see Fox, 1994), but the mean absolute fecundity of bighead goby from the Danube is clearly higher than that in round goby (2109 vs 557), and this is true for virtually all sizes, on a size-class per size-class basis (Table 1). The difference in reproductive strategy between the two species is also reflected in the higher relative fecundity (119.6 vs 54.3; anova, P = 0.0001) and smaller egg diameter observed in female bighead goby relative to those of round goby (1.17 mm vs 1.49 mm; both mean values; anova, P = 0.0001). In both species, these data refer to eggs of the two most mature egg size-groups only, i.e. the eggs spawned within a reproductive season (Table 1) but the difference is also apparent from the frequency distribution of their egg diameters (Fig. 3). Finally, the size at which the two species can reach maturity in the Danube is very similar, though the smallest mature females of bighead goby were slightly smaller than round goby females (42.8 mm vs 45.1 mm LS).

Table 1.   Comparison of absolute fecundity of round Neogobius kesslerei and bighead goby Neogobius melanostomus in the Slovak Danube (in 10 mm SL size classes), including analysis of variance (anova) statistics (respective number of specimens of each species presented as sub-scripts of the F values) and probabilities (P), with significant (P < 0.05) differences highlighted in bold
Fish size class (mm)Round gobyBighead gobyStatistics anovaP-value
MeanSEMeanSE
<60362.0(100.6)763.4(143.1)F11,5 = 5.10.041
61–70336.7(24.7)735.2(81.5)F20,7 = 40.40.000
71–80512.4(54.4)1066.1(129.2)F9,19 = 8.20.008
81–90889.3(227.0)1572.1(218.7)F6,10 = 4.20.060
91–1001043.0(216.9)2303.5(206.0)F2,4 = 14.00.020
101–1102279.9(283.3)
111–1201310.8(131.4)3160.3(287.2)F2,9   = 8.40.018
121–130911.2(627.1)4110.8(725.4)F2,8   = 4.30.071
>1301682.4(99.1)3936.7(1163.9)F2,4   = 1.70.266

Studies devoted to biological invasions generally focus on the possible ecological impact of the invaders on native species and the invaded ecosystems. However, biological invasions can also affect the invader itself, resulting in both genetic and non-genetic changes in the invader. For example, shifts can occur in gene expression, resource allocation (i.e. changes in life-history traits), morphology and physiology within the lifespan of an individual (Strayer et al., 2006). A recent study in which the entire mtDNA cytochrome b gene was sequenced and seven nuclear microsatellite loci were analyzed revealed that the round goby population from the Danube, derived from the Black Sea region, had been initially established with a small founding population. Because of a pronounced founder/bottleneck effect, the genetic diversity (allele frequencies) in this invasive population is strongly limited compared to native populations (Brown and Stepien, 2008). Therefore, changes in the life-history described in non-native round goby from the Danube appear to be non-genetic, and the same can be expected for bighead goby. And, if non-genetic, they then must be epigenetic, because in general the processes of ontogeny derive from two information sources: genetic and epigenetic (e.g. Balon, 2004).

Thus, within the epigenetic concept of alternative ontogenies (Balon, 2004), the available information on the reproductive traits of gobies invading the Danube corroborate the morphological results evaluated in the ontogenetic context (Kováč and Siryová, 2005; Ľavrinčíková et al., 2005) – that the position of invading bighead goby is altricial relative to invading round goby, and this is expressed in less direct ontogeny, higher absolute and relative fecundity and smaller eggs. Furthermore, in both species, a shift from the highly precocial life history of their native populations back towards a more altricial life history in invasive populations has been observed, though this shift seems to be more intensive in bighead goby than in round goby.

The position of a species and/or population on the epigenetic altricial/precocial continuum has some parallels in ecological classifications. For example, altricial forms are less specialised, more adaptable, with higher surplus production of eggs, better coping with unstable environments and unpredictable environmental changes than precocial forms (Balon, 2004). The projection of the described differences in life-history between bighead goby and round goby over the ecological characteristics provides an opportunity for predictions of possible further developments in the population dynamics of these two most abundant and closely-related invaders in the middle Danube area. In other words, these differences, affected by epigenetic mechanisms and resulting in alternative ontogenies, may have important implications for potential success in novel environments, favouring round goby over short time scales (several years), and bighead goby over longer time scales (decades and longer). Naturally, if this prediction turns out to be correct, then the long-term impact of these invaders on Danubian ecosystem will differ considerably between the two species.

Acknowledgement

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References

We thank M. Balážová for her assistance, in particular with literary data and the laboratory processing of the material. C. Stepien kindly provided us information on genetics of non-native gobies from the Danube. This study was funded by VEGA (Slovak Scientific Grant Agency), Projects No. 1/2341/05 and 1/0226/08, with the participation of GHC supported by the UK Department of Environment, Food & Rural Affairs.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgement
  8. References
  • Ahnelt, H.; Bănărescu, P.; Spolwind, R.; Hárka, A.; Waidbacher, H., 1998: Occurrence and distribution of three gobiid species (Pisces, Gobiidae) in the middle and upper Danube region – examples of different dispersal patterns? Biologia 53, 665678.
  • Azizova, N. A., 1962: The possibility of a goby fishery in the Caspian Sea. Ryb. Khozaystvo 3, 14. [In Russian].
  • Balážová-Ľavrinčíková, M.; Kováč, V., 2007: Epigenetic context in the life-history of round goby Neogobius melanostomus from Slovak stretch of the Danube. In: Freshwater bioinvaders: profiles, distribution, and threats. Chapter 14. F.Gherardi (Ed.). Springer, Berlin, pp. 275287.
  • Balon, E. K., 1990: Epigenesis of an epigeneticist: the development of some alternative concepts on the early ontogeny and evolution of fishes. Guelph Ichthyol. Rev. 1, 148.
  • Balon, E. K., 2004: Alternative ontogenies and evolution: a farewell to gradualism. In: Environment, development and evolution, toward a synthesis. B. K.Hall, R. D.Pearson and G. B.Muller (Eds). MIT Press, Cambridge, pp. 3766.
  • Berg, L. S., 1949: Freshwater fishes of the USSR and adjacent countries, Vol. III. Academy of Science USSR, Zoological Institute, Moskva.
  • Brown, J. E.; Steppien, C. A., 2008: Ancient divisions recent expansions: phylogeography and the population genetics of the round goby Apollonia Melanostoma. Molecular Ecology 17, 25982615.
  • Copp, G. H.; Fox, M. G.; Przybylski, M.; Godinho, F.; Vila-Gispert, A., 2004: Life-time growth patterns of pumpkinseed Lepomis gibbosus introduced to Europe relative to native North American populations. Folia Zool. 53, 237254.
  • Copp, G. H.; Bianco, P. G.; Bogutskaya, N.; Erős, T.; Falka, I.; Ferreira, M. T.; Fox, M. G.; Freyhof, J.; Gozlan, R. E.; Grabowska, J.; Kováč, V.; Moreno-Amich, R.; Naseka, A. M.; Peňáz, M.; Povž, M.; Przybylski, M.; Robillard, M.; Russell, I. C.; Stakėnas, S.; Šumer, S.; Vila-Gispert, A.; Wiesner, C., 2005: To be, or not to be, a non-native freshwater fish? J. Appl. Ichthyol. 21, 242262.
  • Fox, M. G., 1994: Growth, density, and interspecific influences on pumpkinseed sunfish life histories. Ecology 75, 11571171.
  • Fox, M. G.; Vila-Gispert, A.; Copp, G.H., 2007: Life history traits of introduced Iberian pumpkinseed (Lepomis gibbosus) relative to native populations: can differences explain colonization success? J. Fish Biol. 71 (Suppl. d), 5669.
  • Georgier, Zh. M., 1996: Vidovij Sostav i charakteristika na popchetata (Gobidae Pisces) v Bulgarii. Isvestia naucho-issle dovatels kovo instituta v ribnostopanii i okeanografii 7. (In Bulgarian).
  • Hoffmeister, T. S.; Vet, L. E. M.; Biere, A.; Holsinger, K.; Filser, J., 2005: Ecological and evolutionary consequences of biological invasion and habitat fragmentation. Ecosystems 8, 657667.
  • Holčík, J.; Hensel, K., 1972: Handbook of ichthyology. Obzor, Bratislava. [In Slovak]
  • Jurajda, P.; Černý, J.; Polačik, M.; Valová, Z.; Janáč, M.; Blažek, R.; Ondračková, M., 2005: The recent distribution and abundance of non-native Neogobius fishes in the Slovak section of the River Danube. J. Appl. Ichthyol. 21, 319323.
  • Kalinina, E., 1976: Reproduction and development of Azov-Black Sea gobies. Naukova Dumka, Kiev, 120 pp.
  • Kováč, V.; Siryová, S., 2005: Ontogenetic variability in external morphology of bighead goby Neogobius kessleri from middle Danube, Slovakia. J. Appl. Ichthyol. 21, 312315.
  • Ľavrinčíková, M.; Kováč, V., 2007: Invasive round goby Neogobius melanostomus from Slovak stretch of the Danube mature at small size. J. Appl. Ichthyol. 23, 276278.
  • Ľavrinčíková, M.; Kováč, V.; Katina, S., 2005: Ontogenetic variability in external morphology of round goby Neogobius melanostomus from middle Danube, Slovakia. J. Appl. Ichthyol. 21, 328334.
  • MacInnis, A. J.; Corkum, L. D., 2000: Fecundity and reproductive seasons of the round goby Neogobius melanostomus in the upper Detroit River. Trans. Am. Fish. Soc. 129, 136144.
  • Pérez, J. E.; Nirchio, M.; Alfonsi, C.; Muñoz, C., 2006: The biology of invasions: the genetic adaption paradox. Biol. Invasions 8, 11151121.
  • Pintér, K., 1998: Die Fische Ungarns, ihre Biologie und Nutzung. Akadémiai Kiadó, Budapest. 230 pp.
  • Ross, S. T., 1991: Mechanisms structuring stream fish assemblages: are there lessons from introduced species? Environ. Biol. Fish 30, 359368.
  • Smirnov, A. I., 1986: Perciformes (Gobioidei), Scorpaeniformes, Pleuronectiformes, Lophiiformes. Fauna Ukrainy 8, Kijev.
  • Stráňai, I., 1999: Fertility of Neogobius kessleri (Günther 1861) from the Slovak part of the Danube River. Czech J. Anim. Sci. 44, 215218.
  • Strayer, D. L.; Eviner, V. T.; Jeschke, J. M.; Pace, M. L., 2006: Understanding the long-term effects of species invasions. Trends Ecol. Evol. 21, 645651.
  • Svetovidov, A. N., 1964: Ryby Tschernovo mora (Fishes of the Black Sea). Nauka, Moscow-Leningrad [in Russian].
  • Tomeček, J.; Kováč, V.; Katina, S., 2007: Biological flexibility of pumpkinseed, a successful coloniser throughout Europe. In: Freshwater bioinvaders: profiles, distribution, and threats. Chapter 16. F.Gherardi (Ed.). Springer, Berlin, pp. 307336.
  • Trifonov, G. P., 1955: To the knowledge on reproductive biology of gobies from the Azov Sea. Trudy Karadag. Biolog. Stancii 13, 546 [In Russian].
  • Zweimuller, I.; Moidl, S.; Nimmervoll, H., 1996: A new species for the Austrian Danube –Neogobius kessleri. Acta Univ. Carol. Biol. 40, 213218.