Timing of the population dynamics of bullhead Cottus gobio (Teleostei: Cottidae) during the Pleistocene

Abstract Pleistocene genetic structure of the bullhead, Cottus gobio, was evaluated across the western Palearctic using a 771‐bp long fragment of the mitochondrial control region in 123 individuals collected at 35 sites (data set I). In total, 59 haplotypes that differed at 73 positions (9.3%) were detected. Data analysis also included sequences from Englbrecht et al. (2000 ), thus increasing the sampling to a more comprehensive data set of 529 fish and 63 control region sequences of 482 bp (data set II). A minimum spanning and phylogenetic tree identified a seventh clade (Brittany–Loire) in addition to the previously identified six clades. The geographical range of the North Sea and Lower Rhine clades was considerably larger than thought previously. Haplotype diversity was generally low, and the total fixation index high (F_ST = 0.49). Among‐group differentiation accounted for 41.7% (data set I) of the variation. Contiguous range expansions and restricted gene flow combined with isolation by distance, interspersed with past fragmentation characterize bullhead across its range. New is the knowledge that dated interglacial periods correlated with population expansions; river captures, proglacial lake systems and sea level played a significant role in the dispersal and expansion either in northern or southern direction. Hence it became possible to identify and date the colonization routes and putative palaeorefugia, most of which were located in Central and North‐west Europe. Glacial periods resulted in distinct fragmentation events and lineage sorting.     

Formation of parasite fauna in the bullhead (Cottus gobio L.) (Pisces: Cottidae)

The formation of parasite fauna in the bullhead Cottus gobio L. in different water bodies was examined. The largest number of parasite species including specific parasites was observed in the Onega and Ladoga lakes. It is suggested that the host and their parasites migrated namely from these water bodies to other part of the range of the bullhead.     

Sound production by the river bullhead, Cottus gobio L. (Cottidae, Teleostei)

Acoustic signals of Cottus gobio consist of knocking sounds produced as single pulses (48 ms) or as trains of 4–6 pulses (230 ms). Frequencies extend up to 3 kHz, but most sound energy is concentrated between 50 and 500 Hz in both sound types. Cottus gobio is solitary, maintains territories, and defends them by threat display, seldom by biting and fighting. Threatening consists of spreading gill covers and fins, darkening, and sound production. Calling is accompanied by a nodding movement of the head, during which the pectoral girdle and the skull are moved rapidly against each other. No difference in ability of sound production was observed between sexes, but males emitted significantly more sounds than females. In the laboratory an increase in vocalization activity was observed between night and day. An increase in the number of encounters and calls was noted when temperatures were raised from 8°C to 13°C. Sound production was registered throughout the year.     

The importance of incorporating age and sex when backcalculating length in bullhead Cottus gobio

The present study backcalculated body length for a data set of a bullhead Cottus gobio population located at different sampling sites in a river network. Model comparison between various growth models, which included successively new parameters, showed the effect and importance of taking sex, age and the location in the river network into account. The data sets obtained by backcalculation were fitted by the von Bertalanffy growth function, which revealed the effect of the backcalculation formula on the estimation of the von Bertalanffy growth parameters. Fitting results and parameter estimates showed again the importance of incorporating age and sex when backcalculating body length in the C. gobio population studied.     

Histological and enzyme histochemical changes in the kidney of male bullhead (Cottus gobio) during the spawning period

Histological and enzyme histochemical studies were carried out on the excretory kidney of the male bullhead ( Cottus gobio ). During the spawning season striking morphofunctional changes were observed in the second proximal segment of the kidney tubule. The tubular epithelium was greatly hypertrophied, strongly basophilic and produced a PAS-positive secretion. The enzyme histochemical pattern also changed conspicuously during this time: the alkaline phosphatase activity in the brush border was greatly reduced; the acid phosphatase and non-specific esterase activity in the cytoplasm was distinctly elevated.     

Gyrodactylus onegensis sp. n. (Monogenea)--a parasite of the bullhead (Cottus gobio L.)

A new species, Gyrodactylus onegensis sp. n., is described from gills of the freshwater sculpin Cottus gobio.     

Concordant genetic estimators of migration reveal anthropogenically enhanced source-sink population structure in the river sculpin, Cottus gobio

River systems are vulnerable to natural and anthropogenic habitat fragmentation and will often harbor populations deviating markedly from simplified theoretical models. We investigated fine-scale population structure in the sedentary river fish Cottus gobio using microsatellites and compared migration estimates from three FST estimators, a coalescent maximum-likelihood method and Bayesian recent migration analyses. Source-sink structure was evident via asymmetry in migration and genetic diversity with smaller upstream locations emigration biased and larger downstream subpopulations immigration biased. Patterns of isolation by distance suggested that the system was largely, but not entirely, in migration-drift equilibrium, with headwater populations harboring a signal of past colonizations and in some cases also recent population bottlenecks. Up- vs. downstream asymmetry in population structure was partly attributable to the effects of flow direction, but was enhanced by weirs prohibiting compensatory upstream migration. Estimators of migration showed strong correspondence, at least in relative terms, especially if pairwise FST was used as an indirect index of relative gene flow rather than being translated to Nm. Since true parameter values are unknown in natural systems, comparisons among estimators are important, both to determine confidence in estimates of migration and to validate the performance of different methods.     

Preliminary observations on different reproduction strategies in the bullhead (Cottus gobio L.) in northern and southern England

The size distribution and numbers of oocytes were examined in samples of ovaries from two sites and in fish in tanks whose past spawning activities were known. In an upland stream in northern England Cottus gobio would seem to be an annual spawner, maturing a single batch of eggs each year. In a more productive stream in southern England, where the reproductive life is short, fish mature and lay a succession of batches of eggs during a long spawning season. The physiological and ecological implications of these characteristics are discussed.     

Genetic analysis of potential postglacial watershed crossings in Central Europe by the bullhead (Cottus gobio L.)

Natural colonizations across watersheds have been frequently proposed to explain the present distributions of many freshwater fish species. However, detailed studies of such potential watershed crossings are still missing. Here, we investigated potential postglacial watershed crossings of the widely distributed European bullhead (Cottus gobio L.) in two different areas along the Rhine–Rhône watershed using detailed genetic analysis. The main advantage of studying bullheads vs. other freshwater fish species is that their distribution has been lightly influenced by human activities and as such, interpretations of colonization history are not confounded by artificial transplantations. The genetic analyses of eight microsatellite loci revealed strong genetic similarities between populations of both sides of the Rhine–Rhône watershed in the Lake Geneva area, giving strong evidence for a natural watershed crossing of bullheads from the upper Rhine drainage into the Rhône drainage in the Lake Geneva area likely facilitated by the retreat of the glaciers after the last glacial maximum some 20 000 years ago. Populations from the Lake Geneva basin were genetically more similar to populations from across the watershed in the upper Rhine drainage than to populations further downstream in the lower Rhône. In contrast, populations from Belfort, an area, which was not covered by ice during the last glacial maximum, showed strong genetic differentiation between populations of the upper Rhine and Rhône drainages. Based on our results on the bullhead, we propose that glacial retreat may have eased the dispersal of numerous European freshwater fish species across several geological boundaries.     

Effects of temperature on biological and biochemical indicators of the life-history strategy of bullhead Cottus gobio

The biological and biochemical effects of temperature on life-history strategy of female bullhead Cottus gobio were investigated. Fish from two populations (Bez Basin, south-east France) experiencing contrasted thermal environments ( i.e . more or less stable) were reared during 4 months at three distinct temperatures (7, 9 or 12° C). Both somatic (soma fresh mass and muscle triglyceride content) and reproductive (gonad fresh mass, fecundity, mean diameter of eggs and gonad triglyceride content) indicators were examined. Mixed models indicated that an increasing temperature had significant negative effects on all life-history indicators except for soma fresh mass. Differences in life-history strategy with regard to muscle and gonad triglyceride contents, however, suggest that populations experiencing more variable thermal environments may be better adapted than others to cope with an increasing temperature. These findings may have important implications for C. gobio populations, within the context of climate warming.     

Mate choice, egg cannibalism and reproductive success in the river bullhead, Cottus gobio L.

The seasonal pattern and individual variation in reproductive success was studied in a population of the river bullhead, Cottus gobio L. Female fecundity and male reproductive success were correlated with body size. Large males were found to breed early in the season when most of the large females spawned. The diameter of eggs found in male nests indicates that females tend to mate with males larger than themselves. The analysis of stomach contents suggests that guarding males cannibalize some of their own eggs. During parental care, the rate of filial cannibalism increases as guarding male body condition deteriorates.     

Sperm structure and motility of the freshwater teleost Cottus gobio

When motility of spermatozoa of Cottos gobio was initiated with distilled water, the motility rate decreased to 0% within 1 min, and significant signs of osmotic alterations were observed at the end of the motility period. By contrast, in 50 mmol 1⁻¹ NaCl solution, the motility rate persisted for 120–140 min. In both distilled water and in 50 mmol 1⁻¹ NaCl solution, the main swimming type of spermatozoa was linear motion during the whole motility period. The initial swimming velocity (50.0 ± 2.1 μm s⁻¹) measured 10 s after motility initiation was similar in both distilled water and in 50 mmol 1⁻¹ NaCl solution. In distilled water, the velocity decreased to <20 μm s⁻¹ (locally motile) during the first minute of the motility phase. In 50 mmol 1⁻¹ NaCl solutions, it remained at a constant level during the first 60 min of the motility period, but then started to decrease to <20 μm s⁻¹ after 120 min. When 5 mmol 1⁻¹ potassium cyanide, antimycin or atractyloside was added to the 50 mmol 1⁻¹ NaCl solution, the motility period was reduced to ≤2min. Ten millimoles per litre 2-deoxy-D-glucose, malonate or a mixture of 5 mmol 1⁻¹ atractyloside and 5 mmol 1⁻¹ carnithine did not effect the duration of the motility period. This indicates that sperm energy metabolism depends mainly on respiration rate and fatty acid metabolism.     

Spawning habitat enhancement in the European bullhead (Cottus gobio), an endangered freshwater fish in degraded lowland rivers

Due to river regulation, the natural habitat of the European bullhead (Cottus gobio) has been degraded and often there is an apparent lack of suitable spawning substrates (hard objects like stones). Addition of artificial structures to degraded habitats may be a very promising tool for habitat enhancement. In this study, we evaluated the use of ceramic tiles as artificial spawning substrates in canalised and (remaining) meandering parts of anthropogenically perturbated lowland rivers in Flanders (northern part of Belgium). Furthermore, we examined whether water depth and velocity were important determinants for the choice of tiles in these different river trajectories. Tiles were successfully used by the bullhead as spawning substrates. In the meandering parts of the river, the number of egg deposits was significantly positively correlated with water depth, while in canalised river parts, water depth and velocity were of no importance for tile usage. In general, supplementation of rivers with artificial substrates like tiles may be a promising, inexpensive and easy-to-use enhancement technique for degraded bullhead spawning habitat.     

Female mate choice,male-male competition and parental care in the river bullhead,Cottus gobio L. (Pisces,Cottidae)

Male body size was tested for its influence on female mate choice, male-male competition and ability to defend broods in the river bullhead, Cottus gobio L., a polygynous fish with paternal care. Females presented with two potential mates of different sizes significantly preferred to spawn with the larger male. Males smaller than, or 1·5 times longer than, the female were rarely selected as mates. Larger males were more successful in defending their brood from conspecifics, which may explain female preference for them. Unmated large males displaced smaller guarding males from their nests and retained the acquired egg masses. Competition between males for nest sites with eggs can be accounted for by the preference of females for males already guarding eggs: by seizing a nest containing egg masses, a male will increase his chance of being chosen.     

The helminth parasites of the bullhead Cottus gobio (L.) and the stone loach Noemacheilus barbatulus (L.) from the River Avon, Hampshire

Specimens of Cottus gobio and Noemacheilus barbatulus from the River Avon, Hampshire, were examined between July 1970 and July 1971. Both fish were found to act as hosts for Nicolla gallica (adult), Pomphorhynchus laevis (adult) and Triaenophorus nodulosus (plerocercoid). The incidence and intensity of infection were lower in N. barbatulus than in C. gobio , and this was related to differences in host diet. A small number of N. barbatulus were also found to harbour Proteocephalus torulosus . Seasonal cycles of incidence and intensity were evident in N. gallica , with a peak occurring in the winter. P. laevis and T. nodulosus showed no such cycles. Increasing host size was associated with a higher infection of both N. gallica and P. laevis , but not T. nodulosus . The diet of the host was considered to be important in influencing this increase. Differences in host reproductive condition affected the population levels of N. gallica only, where an increased parasite burden was evident in gravid female fish. This was considered to influence the observed increase in incidence and intensity of this parasite during the winter. None of the parasites showed any seasonal maturation cycles. There was no evidence of any interactions between the parasite populations. Host diet and the availability of infective larvae were considered to be the most important features influencing the number of parasites which became established, and the rate at which this occurred. Temperature probably acted indirectly on the establishment of N. gallica , by controlling the availability of the larval stages, and also, by influencing the host reproductive condition, on the length of time for which the parasite was retained by the host.     

Colonization history of the Swiss Rhine basin by the bullhead (Cottus gobio): inference under a Bayesian spatially explicit framework

The present distribution of freshwater fish in the Alpine region has been strongly affected by colonization events occurring after the last glacial maximum (LGM), some 20 000 years ago. We use here a spatially explicit simulation framework to model and better understand their colonization dynamics in the Swiss Rhine basin. This approach is applied to the European bullhead ( Cottus gobio ), which is an ideal model organism to study fish past demographic processes since it has not been managed by humans. The molecular diversity of eight sampled populations is simulated and compared to observed data at six microsatellite loci under an approximate Bayesian computation framework to estimate the parameters of the colonization process. Our demographic estimates fit well with current knowledge about the biology of this species, but they suggest that the Swiss Rhine basin was colonized very recently, after the Younger Dryas some 6600 years ago. We discuss the implication of this result, as well as the strengths and limits of the spatially explicit approach coupled to the approximate Bayesian computation framework.     

Phylogeography of the bullhead Cottus gobio (Pisces: Teleostei: Cottidae) suggests a pre-pleistocene origin of the major central European populations

The bullhead Cottus gobio is a small, bottom-dwelling fish consisting of populations that have not been subject to transplantations or artificial stocking. It is therefore an ideal model species for studying the colonization history of central European freshwater systems, in particular with respect to the possible influences of the Pleistocene glaciation cycles. We sampled Cottus populations across most of its distribution range, with a special emphasis on southern Germany where the major European drainage systems are in closest contact. Mitochondrial D-loop sequencing of more than 400 specimens and phylogenetic network analysis allowed us to draw a detailed picture of the colonization of Europe by C. gobio. Moreover, the molecular distances between the haplotypes enabled us to infer an approximate time frame for the origin of the various populations. The founder population of C. gobio stems apparently from the Paratethys and invaded Europe in the Pliocene. From there, the first colonization into central Europe occurred via the ancient lower Danube, with a separate colonization of the eastern European territories. During the late Pliocene, one of the central European populations must have reached the North Sea in a second step after which it then started to colonize the Atlantic drainages via coastal lines. Accordingly, we found very distinct populations in the upper and lower Rhine, which can be explained by the fact that the lower Rhine was disconnected from the upper Rhine until approximately 1 million years ago (Ma). More closely related, but still distinct, populations were found in the Elbe, the Main and the upper Danube, all presumably of Pleistocene origin. Intriguingly, they have largely maintained their population identity, despite the strong disturbance caused by the glaciation cycles in these areas. On the other hand, a mixing of populations during postglacial recolonization could be detected in the lower Rhine and its tributaries. However, the general pattern that emerges from our analysis suggests that the glaciation cycles did not have a major impact on the general population structure of C. gobio in central Europe.