Pungitius Pungitius Research Articles

Building of HSI Model for the Freshwater Type of Nine-Spined Stickleback (<i>Pungitius</i> sp.1) in the Oko River Basin, Ishikawa, Japan

Building of HSI Model for the Freshwater Type of Nine-Spined Stickleback (<i>Pungitius</i> sp.1) in the Oko River Basin, Ishikawa, Japan

Comparison of catch per unit effort among four minnow trap models in the three-spined stickleback (Gasterosteus aculeatus) fishery.

Minnow traps are commonly used in the stickleback (Gasterostidae) fishery, but the potential differences in catch per unit effort (CPUE) among different minnow trap models are little studied. We compared the CPUE of four different minnow trap models in field experiments conducted with three-spined sticklebacks (Gasterosteus aculeatus). Marked (up to 26 fold) differences in median CPUE among different trap models were observed. Metallic uncoated traps yielded the largest CPUE (2.8 fish/h), followed by metallic black nylon-coated traps (1.3 fish/h). Collapsible canvas traps yielded substantially lower CPUEs (black: 0.7 fish/h; red: 0.1 fish/h) than the metallic traps. Laboratory trials further revealed significant differences in escape probabilities among the different trap models. While the differences in escape probability can explain at least part of the differences in CPUE among the trap models (e.g. high escape rate and low CPUE in red canvas traps), discrepancies between model-specific CPUEs and escape rates suggests that variation in entrance rate also contributes to the differences in CPUE. In general, and in accordance with earlier data on nine-spined stickleback (Pungitius pungitius) trapping, the results suggest that uncoated metallic (Gee-type) traps are superior to the other commonly used minnow trap models in stickleback fisheries.

Construction of Ultradense Linkage Maps with Lep-MAP2: Stickleback F2 Recombinant Crosses as an Example.

High-density linkage maps are important tools for genome biology and evolutionary genetics by quantifying the extent of recombination, linkage disequilibrium, and chromosomal rearrangements across chromosomes, sexes, and populations. They provide one of the best ways to validate and refine de novo genome assemblies, with the power to identify errors in assemblies increasing with marker density. However, assembly of high-density linkage maps is still challenging due to software limitations. We describe Lep-MAP2, a software for ultradense genome-wide linkage map construction. Lep-MAP2 can handle various family structures and can account for achiasmatic meiosis to gain linkage map accuracy. Simulations show that Lep-MAP2 outperforms other available mapping software both in computational efficiency and accuracy. When applied to two large F2-generation recombinant crosses between two nine-spined stickleback (Pungitius pungitius) populations, it produced two high-density (∼6 markers/cM) linkage maps containing 18,691 and 20,054 single nucleotide polymorphisms. The two maps showed a high degree of synteny, but female maps were 1.5–2 times longer than male maps in all linkage groups, suggesting genome-wide recombination suppression in males. Comparison with the genome sequence of the three-spined stickleback (Gasterosteus aculeatus) revealed a high degree of interspecific synteny with a low frequency (<5%) of interchromosomal rearrangements. However, a fairly large (ca. 10 Mb) translocation from autosome to sex chromosome was detected in both maps. These results illustrate the utility and novel features of Lep-MAP2 in assembling high-density linkage maps, and their usefulness in revealing evolutionarily interesting properties of genomes, such as strong genome-wide sex bias in recombination rates.

Taste preferences and feeding behavior in nine-spined stickleback (Pungitius pungitius) in three geographically distant populations

Taste preferences of classical taste substances (10% each sodium chloride, calcium chloride, and sucrose; and 5% citric acid), and 21 free amino acids (L-isomers, 0.1–0.001 M) and feeding behavior of the nine-spined stickleback Pungitius pungitius belonging to the populations of the Moskva River (Caspian Sea basin), Lake Mashinnoe (White Sea, Kandalaksha Gulf), and Bol’shaya River (Western Kamchatka, Okhotsk Sea) are determined. It is proven that the spectra of taste preferences are similar in different stickleback populations. For sticklebacks in all three populations, citric, aspartic, and glutamic acids are mostly palatable. The maximum number of palatable amino acids (16) is found in sticklebacks from the Moskva River. Sticklebacks from the White and Okhotsk seas prefer the lower number of amino acids, 10 and 4, respectively. Deterrent amino acids are not found. The gustatory amino acid spectra of sticklebacks from different populations are positively correlated (p < 0.05). Sticklebacks from the Sea of Okhotsk relatively rare taste the offered food objects again (agar–agar pellets with the studied taste substances). Such behavior is more common in sticklebacks from the White Sea, and those from the Moskva River have an intermediary position. The manipulation activity in the compared fish is associated with the hydrology of the water bodies. In ninespined sticklebacks from all three populations, the actions performed upon intra-oral testing of a food object follow two alternative behavioral stereotypes. The stereotypes of swallowing and of rejection of food differ slightly between the populations and depend on the palatability of the offered object.

Baiting improves CPUE in nine-spined stickleback (Pungitius pungitius) minnow trap fishery.

Whether or not baiting influences stickleback catch per unit effort (CPUE) remains a matter of debate among stickleback researchers: While the opinions about the impact of baiting on CPUE differ, supporting quantitative data are scarce. The effect of baiting and trap type on nine-spined stickleback (Pungitius pungitius) CPUE was studied in a field experiment conducted over four consecutive days in a small pond in northeastern Finland. The results show that baited traps yielded better (mean CPUE = 1.24 fish/trap/d) catches than unbaited traps (mean CPUE = 0.66); however, there were also differences in CPUE depending on the type of collapsible trap that was used. The trap type effect on CPUE seemed to differ among age classes – the finer meshed trap caught more young-of-the-year fish than the coarse-meshed one, whereas the opposite was true for the older and larger individuals. The results agree with those of an earlier more restricted study conducted in the same locality: Together, these results provide strong evidence for the positive impact of baiting on nine-spined stickleback CPUE.

Spatial and temporal variation in fish assemblages in three small unpolluted estuarine rivers and associated lagoons in Kouchibouguac National Park, southern Gulf of St. Lawrence, Canada

Estuaries have among the highest primary production rates of ocean waters and provide essential habitat for many organisms. Recognition of the need to conserve these critical habitats is coupled with the need for baseline data to allow assessment of ecosystem changes. This study compares natural variations in, and correlations between, the composition of fish assemblages and environmental factors at several sites over two years in three rivers emptying into estuaries in the southern Gulf of St. Lawrence, Canada. Fish diversity and abundance were determined by beach seining and related to water temperature, salinity, substrate, and vegetation. From May to September 2000 (14 sites) and May to August 2001 (15 sites), 20 fish species were collected, seven of which accounted for 98% of the total catch. The dominant species, Mummichog (Fundulus heteroclitus), represented 44% of the catch. Its abundance and that of the other dominant species — Threespine Stickleback (Gasterosteus aculeatus) 16%, Blackspotted Stickleback (G. wheatlandi) 13%, Banded Killifish (F. diaphanus) 12%, Fourspine Stickleback (Apeltes quadracus) 7%, Atlantic Silverside (Menidia menidia) 4%, and Ninespine Stickleback (Pungitius pungitius) 2% — differed significantly both spatially and temporally. Multidimensional scaling analysis showed a spatial gradient in abundance from upstream to lagoon sites and a temporal gradient from spring to fall. Upstream sites were low in salinity and had a higher organic content and a higher proportion of silt–clay in the sediment. Variation within fish populations was related to site and seasonal changes in environmental conditions and species’ tolerance of water temperature, salinity, vegetation coverage, and fine sediments.

Persistent Organochlorine Pesticide Exposure Related to a Formerly Used Defense Site on St. Lawrence Island, Alaska: Data from Sentinel Fish and Human Sera

St. Lawrence Island, Alaska, is the largest island in the Bering Sea, located 60 km from Siberia. The island is home to approximately 1600 St. Lawrence Island Yupik residents who live a subsistence way of life. Two formerly used defense sites (FUDS) exist on the island, one of which, Northeast Cape, has been the subject of a $123 million cleanup effort. Environmental monitoring demonstrates localized soil and watershed contamination with polychlorinated biphenyls (PCB), organochlorine (OC) pesticides, mercury, and arsenic. This study examined whether the Northeast Cape FUDS is a source of exposure to OC pesticides. In total, 71 serum samples were collected during site remediation from volunteers who represented three geographic regions of the island. In addition, ninespine stickleback (Pungitius pungitius) and Alaska blackfish (Dallia pectoralis) were collected from Northeast Cape after remediation to assess continuing presence of OC pesticides. Chlordane compounds, DDT compounds, mirex, and hexachlorobenzene (HCB) were the most prevalent and present at the highest concentrations in both fish tissues and human serum samples. After controlling for age and gender, activities near the Northeast Cape FUDS were associated with an increase in serum HCB as compared to residents of the farthest village from the site. Positive but nonsignificant relationships for sum-chlordane and sum-DDT were also found. Organochlorine concentrations in fish samples did not show clear geographic trends, but appear elevated compared to other sites in Alaska. Taken together, data suggest that contamination of the local environment at the Northeast Cape FUDS may increase exposure to select persistent OC pesticides.

Consistent isotopic differences between Schistocephalus spp. parasites and their stickleback hosts.

Parasite-host systems show markedly variable patterns in isotopic fractionation: parasites can be either depleted or enriched in ¹⁵N and ¹³C as compared to their hosts. However, it remains unknown whether isotopic fractionation patterns are similar in comparable parasite-host systems from markedly different ecosystems. Results of this study show that large-sized Schistocephalus spp. endoparasites are consistently depleted in ¹⁵N (by on average -2.13 to -2.20 ‰) as compared to their nine-spined stickleback Pungitius pungitius and three-spined stickleback Gasterosteus aculeatus hosts. The differences between parasites and host for both δ¹⁵N and δ¹³C were consistent in both study systems despite marked biogeographical differences between the study localities. Although the stable isotope values in general were strongly correlated between the hosts and their parasites, Schistocephalus specimens occupying the same nine-spined stickleback host showed sometimes substantial individual variation in δ¹³C. This might be due to selective use of different carbon sources, or different metabolic or feeding rates. Further studies on selective feeding, physiology and metabolism of parasites are needed to better understand the role of parasites in the structure and functioning of aquatic food webs.

Population genetic structure and colonization history of short ninespine sticklebacks (Pungitius kaibarae).

The contemporary distribution and genetic structure of a freshwater fish provide insight into its historical geodispersal and geographical isolation following Quaternary climate changes. The short ninespine stickleback, Pungitius kaibarae, is a small gasterosteid fish occurring in freshwater systems on the Korean Peninsula and in southeast Russia. On the Korean Peninsula, P. kaibarae populations are distributed in three geographically separated regions: the NE (northeast coast), SE (southeast coast), and a limited area in the ND (Nakdong River). In this study, we used mitochondrial loci and microsatellites to investigate the evolutionary history of P. kaibarae populations by assessing their pattern of genetic structure. Our analyses revealed a marked level of divergence among three regional populations, suggesting a long history of isolation following colonization, although ND individuals showed relatively higher genetic affinity to populations from SE than those from NE. The populations from NE showed a great degree of interpopulation differentiation, whereas populations from SE exhibited only weak genetic structuring. Upon robust phylogenetic analysis, P. kaibarae formed a monophyletic group with Russian P. sinensis and P. tymensis with strong node confidence values, indicating that P. kaibarae populations on the Korean Peninsula originated from the southward migration of its ancestral lineage around the middle Pleistocene.

To what extent do human-altered landscapes retain population connectivity? Historical changes in gene flow of wetland fish Pungitius pungitius.

Understanding how human-altered landscapes affect population connectivity is valuable for conservation planning. Natural connectivity among wetlands, which is maintained by floods, is disappearing owing to farmland expansion. Using genetic data, we assessed historical changes in the population connectivity of the ninespine stickleback within a human-altered wetland system. We predicted that: (i) the contemporary gene flow maintained by the artificial watercourse network may be restricted to a smaller spatial scale compared with the gene flow preceding alteration, and (ii) the contemporary gene flow is dominated by the downstream direction owing to the construction of low-head barriers. We evaluated the potential source population in both timescales. Seventeen studied populations were grouped into four genetically different clusters, and we estimated the migration rates among these clusters. Contemporary migration was restricted to between neighbouring clusters, although a directional change was not detected. Furthermore, we consistently found the same potential source cluster, from past to present, characterized by large amounts of remnant habitats connected by artificial watercourses. These findings highlight that: (i) artificial connectivity can sustain the short-distance connectivity of the ninespine stickleback, which contributes to maintaining the potential source populations; however, (ii) population connectivity throughout the landscape has been prevented by agricultural developments.

Space-use and sociability are not related to public-information use in ninespine sticklebacks

There has been much recent interest in both public information use, and the evolutionary origins and ecological consequences of animal personalities but surprisingly little integration of these two fields. Personality traits may impact upon the extent to which individuals respond to public information in a number of different ways. As a first step towards addressing some of these questions, in this study, we asked whether personality traits predicted public information use in ninespine sticklebacks (Pungitius pungitius). Over a 33-day period, subjects were scored twice for a number of behavioural traits, including measures of activity, exploration and shoaling tendency, and were exposed multiple times to a public information use foraging task, in which they were required to select the richer of two prey patches based upon the foraging success of two demonstrator groups. The repeatable (r = 0.38–0.58) behavioural traits were reduced to two principle components describing space use and sociability. Neither of these was found to be related to either of two measures of public information use. While the personality traits that we considered did not co-vary with public information use in this species, they may well indirectly affect opportunity for exposure to public information, and this is an obvious avenue for further research.

Winter feeding ecology and the importance of cannibalism in juvenile and adult burbot (Lota lota) from the Mackenzie Delta, Canada

The diet of adult burbot (Lota lota) collected from two locations in the Mackenzie Delta during the winter was characterized using stomach content and stable isotopes analysis (δ 13C and δ 15N). Burbot consumed mainly ninespine stickleback, juvenile northern pike, and conspecifics, with high δ 15N confirming long-term piscivory. Of the 66 adult burbot sampled, 530 juvenile burbot were enumerated from their stomachs, and from these, 50 juvenile burbot were counted. Many of these juveniles were undigested and were examined for diet content and stable isotopes. Juveniles primarily consumed invertebrates, however, piscivory was detected in young-of-the-year, with stickleback and conspecifics becoming more important as size increased, possibly resulting in competition with adults for small-size fish. δ 15N indicated juvenile burbot occupied a lower tropic level while δ 13C suggested differences in habitat properties between sites. Cannibalism was important to adult diet where the highest frequency of occurrence was 96%, with conspecifics accounting for 82 and 93% of diet items by number and weight, respectively. Cannibalism in burbot increased its trophic breadth and juvenile growth rate, and combined with the amount of conspecifics consumed possibly promoted population stability and coexistence with intraguild predators.

Morphological and ecological variation among populations and subspecies of Burbot (&lt;em&gt;Lota lota&lt;/em&gt; [L, 1758]) from the Mackenzie River Delta, Canada

The Burbot (Lota lota [L, 1758]) is a holarctic distributed freshwater fish in the Gadidae family. In northwestern Canada, it has an important value for local and traditional fisheries. We describe the morphology and ecology of Burbot from four populations in the Mackenzie River Delta. Two subspecies come into contact in this area, which is the western edge of Lota lota maculosa distribution (one population in our study) and the eastern edge of Lota lota lota distribution (three populations in our study). We found the combined length–weight relationship in these four populations to be log10 (weight) = −3.986 + 2.617 * log10 (length). There was no difference in mean body length (overall mean and standard deviation 73.4 ± 8.7 cm), although the L. l. lota populations were heavier than the L. l. maculosa population. All populations differed in their carbon and nitrogen stable isotope signatures (δ15N overall mean 12.1 ± 1.59; δ13C overall mean −25.54 ± 1.11). Main prey items were four fish species: Ninespine Stickleback (Pungitius pungitius [L, 1758]), Broad Whitefish (Coregonus nasus [Pallas, 1776]), Burbot, and Northern Pike (Esox lucius [L, 1758]). Ecological and morphological differences may be due to local conditions and population variability or to the different Lota lota subspecies. More ecological and morphological information from this region is needed to resolve possible phenotypic differences between the subspecies.

Diet shifts by planktivorous and benthivorous fishes in northern Lake Michigan in response to ecosystem changes

In Lake Michigan, diets of planktivorous and benthivorous fishes have varied over the past decades, in part owing to food web changes. To update diet information and compare them to a similar effort in 1994–1995, we analyzed the diets of seven benthivorous and planktivorous fish species collected along two northern Lake Michigan transects that spanned nearshore (18 m), intermediate (46 m), and offshore (91, 110, 128 m) bottom depths during spring, summer, and autumn of 2010. Calanoid copepods (e.g., Limnocalanus macrurus, Leptodiaptomus sicilis, and Senecella calanoides) comprised a majority of the diets in at least one season for all sizes of alewife (Alosa pseudoharengus), bloater (Coregonus hoyi), and rainbow smelt (Osmerus mordax). Similarly, Mysis diluviana was the highest proportion in at least one season for large sizes of alewife, bloater, and rainbow smelt, as well as slimy sculpin (Cottus cognatus) and deepwater sculpin (Myoxocephalus thompsonii). The diets of the remaining two species, ninespine stickleback (Pungitius pungitius) and round goby (Neogobius melanostomus), were dominated by herbivorous cladocerans or dreissenid mussels, respectively. Interspecific diet overlap was minimal at 18 and 46 m. In offshore waters, however, overlap was relatively high, driven by frequent consumption of Mysis. Relative to 1994–1995, 2010 diets revealed increased feeding on calanoid copepods and Mysis, with corresponding declining consumption of Diporeia spp. and herbivorous cladocerans. Relative diet weight was also higher in 1994–1995 than in 2010 for small and large bloater and both sculpin species. We hypothesize that the shifts in diets are reflective of community-level changes in invertebrate prey availability.

Public information use by foraging ninespine sticklebacks: Social learning or an unlearned social influence on travel direction?

If we are to understand the cognitive basis and evolutionary origins of a particular behaviour, it is necessary to identify its underlying mechanism. Ninespine sticklebacks (Pungitius pungitius) can identify the richer of two prey patches by observing other foragers’ success. This may be due to social learning, or an unlearned social effect on travel direction, brought about by the fish being more likely to face and subsequently travel towards areas where they have observed more feeding activity. Here we show that observer orientation does not predict patch choice, and that fish are still more likely to spend more time in richer patches even if they have to take an indirect route to reach them. This suggests that sticklebacks can learn the location of the richer patch through observation, and viewed in conjunction with other published findings, suggests that learned local enhancement lies behind public information use in this species.

Monitoring of Pool and Weir Fishway with Orifices for Freshwater Type of Nine-Spined Stickleback

Monitoring of Pool and Weir Fishway with Orifices for Freshwater Type of Nine-Spined Stickleback

Differential effects of spatial network structure and scale on population size and genetic diversity of the ninespine stickleback in a remnant wetland system

Summary The management of population size and genetic diversity in fragmented landscapes is the central issue in conservation biology. Functional connectivity between remnant habitat patches affects these parameters. However, the functional connectivity for genetic diversity would be characterised by a greater spatial scale than population size even within the same habitat network. The reason for this difference is that while dispersal frequency generally decreases with increasing distance, only a few immigrants may effectively contribute to gene flow, whereas a certain number of dispersers may be required to influence population abundance. Here, we investigated the effects of habitat network structures on population abundance and genetic diversity of the ninespine stickleback, Pungitius pungitius, in remnant wetland ponds in northern Japan. We tested (i) whether both population abundance and genetic diversity are positively related not only to habitat size but also to connectivity and (ii) whether the dispersal effect extends to greater spatial scales in genetic diversity than in population size. We employed a graph theoretical index to measure the degree of pond connectivity. This index can evaluate the connectivity threshold distance above which individuals cannot disperse and clarify the difference in the spatial scale of effective dispersal between population abundance and genetic diversity. Pond connectivity significantly affected the spatial variation of both population abundance and genetic diversity. In contrast, pond size was related only to population abundance. As we predicted, the connectivity threshold distance for genetic diversity was more than two times greater than that for population abundance (12.5 km versus 5 km, respectively). Our findings indicate that the landscape managers should consider various spatial scales as a conservation unit for the management of a habitat network in accordance with the conservation targets that they establish. We also found that small artificial agricultural ditches and streams may play important roles in sustaining the population networks of wetland organisms.

Population divergence in compensatory growth responses and their costs in sticklebacks.

Compensatory growth (CG) may be an adaptive mechanism that helps to restore an organisms’ growth trajectory and adult size from deviations caused by early life resource limitation. Yet, few studies have investigated the genetic basis of CG potential and existence of genetically based population differentiation in CG potential. We studied population differentiation, genetic basis, and costs of CG potential in nine-spined sticklebacks (Pungitius pungitius) differing in their normal growth patterns. As selection favors large body size in pond and small body size in marine populations, we expected CG to occur in the pond but not in the marine population. By manipulating feeding conditions (viz. high, low and recovery feeding treatments), we found clear evidence for CG in the pond but not in the marine population, as well as evidence for catch-up growth (i.e., size compensation without growth acceleration) in both populations. In the marine population, overcompensation occurred individuals from the recovery treatment grew eventually larger than those from the high feeding treatment. In both populations, the recovery feeding treatment reduced maturation probability. The recovery feeding treatment also reduced survival probability in the marine but not in the pond population. Analysis of interpopulation hybrids further suggested that both genetic and maternal effects contributed to the population differences in CG. Hence, apart from demonstrating intrinsic costs for recovery growth, both genetic and maternal effects were identified to be important modulators of CG responses. The results provide an evidence for adaptive differentiation in recovery growth potential.

Differences in the metabolic response to temperature acclimation in nine-spined stickleback (Pungitius pungitius) populations from contrasting thermal environments.

Metabolic responses to temperature changes are crucial for maintaining the energy balance of an individual under seasonal temperature fluctuations. To understand how such responses differ in recently isolated populations (<11,000 years), we studied four Baltic populations of the nine-spined stickleback (Pungitius pungitius L.) from coastal locations (seasonal temperature range, 0-29°C) and from colder, more thermally stable spring-fed ponds (1-19°C). Salinity and predation pressure also differed between these locations. We acclimatized wild-caught fish to 6, 11, and 19°C in common garden conditions for 4-6 months and determined their aerobic scope and hepatosomatic index (HSI). The freshwater fish from the colder (2-14°C), predator-free pond population exhibited complete temperature compensation for their aerobic scope, whereas the coastal populations underwent metabolic rate reduction during the cold treatment. Coastal populations had higher HSI than the colder pond population at all temperatures, with cold acclimation accentuating this effect. The metabolic rates and HSI for freshwater fish from the pond with higher predation pressure were more similar to those of the coastal ones. Our results suggest that ontogenic effects and/or genetic differentiation are responsible for differential energy storage and metabolic responses between these populations. This work demonstrates the metabolic versatility of the nine-spined stickleback and the pertinence of an energetic framework to better understand potential local adaptations. It also demonstrates that instead of using a single acclimation temperature thermal reaction norms should be compared when studying individuals originating from different thermal environments in a common garden setting.

Genome-wide linkage disequilibrium in nine-spined stickleback populations.

Variation in the extent and magnitude of genome-wide linkage disequilibrium (LD) among populations residing in different habitats has seldom been studied in wild vertebrates. We used a total of 109 microsatellite markers to quantify the level and patterns of genome-wide LD in 13 Fennoscandian nine-spined stickleback (Pungitius pungitius) populations from four (viz. marine, lake, pond, and river) different habitat types. In general, high magnitude (D’ > 0.5) of LD was found both in freshwater and marine populations, and the magnitude of LD was significantly greater in inland freshwater than in marine populations. Interestingly, three coastal freshwater populations located in close geographic proximity to the marine populations exhibited similar LD patterns and genetic diversity as their marine neighbors. The greater levels of LD in inland freshwater compared with marine and costal freshwater populations can be explained in terms of their contrasting demographic histories: founder events, long-term isolation, small effective sizes, and population bottlenecks are factors likely to have contributed to the high levels of LD in the inland freshwater populations. In general, these findings shed new light on the patterns and extent of variation in genome-wide LD, as well as the ecological and evolutionary factors driving them.