Brook Lamprey Research Articles

THE ROLE OF STREAMS OF DIFFERENT SIZES IN RECOVERY OF FISH FAUNA IN THE PILICA RIVER CATCHMENT

Fish and lampreys were sampled by electrofishing in the Pilica River tributaries (the Vistula catchment, Poland) in 1992–1994 and 2003–2005. The patterns in fish assemblages were recognized on the basis of fish biomass using Kohonen's self-organizing map (SOM) technique, combined with the indicator values (IndVal) for assessment of associations of fish species with particular SOM regions (and respective environmental conditions). Although the fish samples were clustered mostly according to the stream features (size, regulation, and pollution), a weaker temporal gradient indicated a recovery of the ichthyofauna in some smaller streams. The larger tributaries served as sources of colonisers for both the Pilica and the smaller streams. The differences between SOM subclusters in the quality of the aquatic environment were effectively presented with certain biological measures, including the dominances of potentially large species and non-psammophilous rheophils, which are proposed as good bioindicators. It is worth mentioning that some closely related species (ide and dace, silver bream and bream, golden loach and spined loach, and Ukrainian lamprey and brook lamprey) were significantly associated with different SOM regions (and respective environmental conditions), perhaps in this way avoiding competition. Copyright © 2013 John Wiley & Sons, Ltd.

자연산 다묵장어, Lethenterone reissneri에서 발생한 물곰팡이병 원인체의 동정

자연산 다묵장어, Lethenterone reissneri에서 발생한 물곰팡이병의 원인체를 형태학적 및 유전학적 연구를 통하여 동정하였다. 분리균주는 격벽이 없는 균사를 형성하였고, 가늘고 긴 모양의 유주자낭 내에 활발한 운동성을 보이는 유주자가 여러 줄로 배열되었다가 유주자낭의 선단에서 휴면하지 않고 한꺼번에 방출되는 특징을 보였다. 한편 유성생식기관인 조란기와 조정기는 관찰되지 않았다. 또한 분리균주의 ITS sequence를 분석하고 Saprolegnia 속의 다른 분리균주와 유전학적 상관관계를 조사한 결과, S. parasitica가 속해있는 clade I에 분류되는 것을 확인할 수 있었다. 무성생식기관의 형태, 유주자 방출방식 및 ITS sequence의 phylogenetic analysis에 근거하여 자연산 다묵장어에서 관찰된 물곰팡이병의 원인체는 S. parasitica인 것으로 동정되었다. Saprolegnia isolate from wild brook lamprey was identified on the basis of its morphological and molecular characteristics. The isolates showed aseptic hyphae and clavate zoosporagium. Zoospores discharge was typically saprolegnoid. Neither oogomia nor antheridia was observed in this study. ITS sequence obtained from the isolate was compared with other Saprolegnia spp. to analyse their phylogenetic relationships. Results showed that the isolate belongs to clade I including Saprolegnia parasitica. Based on the asexual organs, zoospore discharge manner and ITS sequence analysis, the isolate was identified as S. parasitica.

Organization of lampreyvariable lymphocyte receptor Clocus and repertoire development

Jawless vertebrates are pivotal representatives for studies of the evolution of adaptive immunity due to their unique position in chordate phylogeny. Lamprey and hagfish, the extant jawless vertebrates, have an alternative lymphocyte-based adaptive immune system that is based on somatically diversifying leucine-rich repeat (LRR)-based antigen receptors, termed variable lymphocyte receptors (VLRs). Lamprey T-like and B-like lymphocyte lineages have been shown to express VLRA and VLRB types of anticipatory receptors, respectively. An additional VLR type, termed VLRC, has recently been identified in arctic lamprey (Lethenteron camtschaticum), and our analysis indicates that VLRC sequences are well conserved in sea lamprey (Petromyzon marinus), L. camtschaticum, and European brook lamprey (Lampetra planeri). Genome sequences of P. marinus were analyzed to determine the organization of the VLRC-encoding locus. In addition to the incomplete germ-line VLRC gene, we have identified 182 flanking donor genomic sequences that could be used to complete the assembly of mature VLRC genes. Donor LRR cassettes were classifiable into five basic structural groups, the composition of which determines their order of use during VLRC assembly by virtue of sequence similarities to the incomplete germ-line gene and to one another. Bidirectional VLRC assembly was predicted by comparisons of mature VLRC genes with the sequences of donor LRR cassettes and verified by analysis of partially assembled intermediates. Biased and repetitive use of certain donor LRR cassettes was demonstrable in mature VLRCs. Our analysis provides insight into the unique molecular strategies used for VLRC gene assembly and repertoire diversification.

Influence of macrohabitat preferences on the distribution of European brook and river lampreys: Implications for conservation and management

The European river lamprey, Lampetra fluviatilis (L.), and the European brook lamprey, Lampetra planeri (Bloch, 1784), are considered highly threatened in Portugal. However, the lack of information about the ecology and distribution of these species poses difficulties to the identification of concrete actions directed to their conservation. A total of 401 sampling sites, randomly distributed throughout the entire Portuguese mainland territory were selected, and Lampetra sp. ammocoetes presence or absence checked with electrofishing. These data, together with 11 macrohabitat predictors, were analyzed using Boosted Regression Trees (BRTs). The BRT models consistently identified five environmental variables as the most important for predicting the distribution of European brook and river lamprey ammocoetes: altitude, distance to coast, sand, maximum temperature of the warmest month and precipitation of the driest month. The relationships of these variables with the species probability of occurrence suggest that lampreys occur in low altitude river stretches (<170m), relatively close to the coast (<150km) and with a sandy substrate (>70% sand). In addition, intermediate values of temperature and precipitation were also found to have a positive correlation with the species occurrence. A map with the probability of occurrence of Lampetra sp. in Portugal was generated and stretches of rivers were delimited with different conservation priorities. Rivers classified with the highest level of conservation priority were considered to be proposed as Special Areas of Conservation, under the Natura 2000 Networking Programme.

Early Spawning by the American Brook Lamprey (&lt;em&gt;Lethenteron appendix&lt;/em&gt;) in Southeastern Minnesota

Record-setting warm temperatures in the upper Midwest during early 2012 resulted in early spawning by the American Brook Lamprey (Lethenteron appendix) in southeastern Minnesota. American Brook Lampreys in a total of five streams in three drainages spawned up to one month earlier than typical. Mean day of year of spawning groups observed in 2012 was significantly different from the mean for groups observed during the period 2002–2010, but mean water temperature was not significantly different. Limited historical data are not sufficient to show an effect of climate change on spawning phenology because some data are confounded with the effects of latitude and year-to-year variability in thermal regime.

Distribution of Pacific LampreyEntosphenus tridentatusin Watersheds of Puget Sound Based on Smolt Monitoring Data

Abstract Lamprey populations are in decline worldwide and the status of Pacific lamprey (Entosphenus tridentatus) is a topic of current interest. They and other lamprey species cycle nutrients and serve as prey in riverine ecosystems. To determine the current distribution of Pacific lamprey in major watersheds flowing into Puget Sound, Washington, we sampled lamprey captured during salmonid smolt monitoring that occurred from late winter to mid-summer. We found Pacific lamprey in 12 of 18 watersheds and they were most common in southern Puget Sound watersheds and in watersheds draining western Puget Sound (Hood Canal). Two additional species, western brook lamprey (Lampetra richardsoni) and river lamprey (L. ayresii) were more common in eastern Puget Sound watersheds. Few Pacific lamprey macrophthalmia were found, suggesting that the majority of juveniles migrated seaward during other time periods. In addition, “dwarf” adult Pacific lamprey (< 300 mm) were observed in several watersheds and may represent ...

ASPECTS OF BROOK LAMPREY (LAMPETRA PLANERI BLOCH) SPAWNING IN IRISH WATERS

Surveying of brook lamprey (Lampetra planen Bloch) spawning activity was undertaken within a number of Irish river catchments during 2004-2011. Presence of adult fish, redd construction and spawning activity is reported. Additional data pertaining to spawning redd physical attributes and riverine conditions were collected at selected sites. Lampetra planen redds were, in general, relatively shallow excavations, averaging 3.5cm depth into the river bed substrate. Redds were typically 8-10cm in diameter with excavated substrate generally forming low mounds, 1-2cm in height, immediately downstream. Active redds were most frequently located in shallow (≤ 10cm water depth) fast-flowing (0.20m s⁻¹ ) sections of watercourses. Because of excavation, water velocities were significantly lower inside redd structures when compared with velocities outside. Implications for conservation monitoring are discussed.

Three new cryptic species of the lamprey genus Lampetra Bonnaterre, 1788 (Petromyzontiformes: Petromyzontidae) from the Iberian Peninsula

The Iberian Peninsula is a repository for biodiversity, presenting high levels of endemism in both plants and animals. In this peninsular region, brook lampreys confined to small, isolated river basins evolved in allopatry giving rise to evolutionary lineages, as revealed by mitochondrial DNA markers. For a better understanding of the taxonomic status and relationships of Iberian populations of the genus Lampetra, we combined previous data from genetics and morphological analysis (assessed here), and describe three new species of the lamprey genus Lampetra Bonnaterre, 1788 in Portugal. In this region L. planeri actually represent a complex of cryptic species, each having smaller geographic ranges than L. planeri, and consequently, greater vulnerability to extinction. The description of Lampetra alavariensis sp. nov. is based on 36 specimens collected on Ribeira de Mangas, a tributary of river Esmoriz, in Northern Portugal. Lampetra auremensis sp. nov. is described on the basis of 31 specimens collected on Ribeira do Olival, a small tributary of river Nabão (Tagus basin). Finally, Lampetra lusitanica sp. nov. is described based on 38 specimens from Ribeira da Marateca, Sado river basin, the southernmost distribution of the genus Lampetra. The recognition of these new species will contribute to the conservation of these already imperilled taxa and will help prevent the extinction of three important evolutionary lineages.

Post-zygotic hybrid viability in sympatric species pairs: a case study from European lampreys

Ecological speciation mechanisms are widely assumed to play an important role in the early stages of divergence between incipient species, and this especially true of fishes. In the present study, we tested explicitly for post-zygotic barriers to gene flow between a sympatric, recently diverged lamprey species pair that likely arose through ecological divergence. Experimental in vitro hybridization between anadromous parasitic Lampetra fluviatilis and resident nonparasitic Lampetra planeri resulted in a high proportion of embryos capable of attaining the burrowing pro-larval stage, strongly indicating no post-zygotic barriers to gene flow between these species. A sympatric, locally-adapted resident parasitic form of L. fluviatilis was also found to successfully hybridize with both members of this species pair. The consequences of these findings are discussed in the context of lamprey speciation. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 108, 378–383.

Functional and evolutionary implications of the cellular composition of the gill epithelium of feeding adults of a freshwater parasitic species of lamprey, Ichthyomyzon unicuspis

This paper provides the first description of the cellular composition of the gill epithelium of feeding adults of Ichthyomyzon unicuspis Hubbs and Trautman, 1937 (silver lamprey), a parasitic species of lamprey that is confined to fresh water. The surface layer of this epithelium consists solely of pavement cells and intercalated mitochondria-rich cells, which are the only cell types found in all freshwater stages of lampreys and thus considered responsible for the uptake of Na+ and Cl– in hypotonic environments. This epithelium does not contain, however, the chloride cells present during the marine parasitic phase of anadromous lamprey species, such as Petromyzon marinus L., 1758 (sea lamprey), and which are responsible for secreting excess Na+ and Cl–. The absence of this cell type in parasitic adults of I. unicuspis also differs from its presence in parasitic adults of landlocked P. marinus and metamorphosing individuals of the exclusively freshwater nonparasitic species Lethenteron appendix (DeKay, 1842) (American brook lamprey), and which thus reflects the retention of a cell type that was crucial for osmoregulation during the marine phase of their respective anadromous parasitic ancestors. The absence of chloride cells in I. unicuspis is consistent with the hypothesis that Ichthyomyzon, which is at or close to the base of the phylogenetic tree for Northern Hemisphere lampreys (Petromyzontidae), evolved in fresh water or has been confined to fresh water for a very long period.

Genetic diversity, endemism and phylogeny of lampreys within the genus Lampetra sensu stricto (Petromyzontiformes: Petromyzontidae) in western North America

Phylogenetic structure of four Lampetra species from the Pacific drainage of North America (western brook lamprey Lampetra richardsoni, Pacific brook lamprey Lampetra pacifica, river lamprey Lampetra ayresii and Kern brook lamprey Lampetra hubbsi) and unidentified Lampetra specimens (referred to as Lampetra sp.) from 36 locations was estimated using the mitochondrial cytochrome b gene. Maximum parsimony and Bayesian inferences did not correspond with any taxonomic scheme proposed to date. Rather, although L. richardsoni (from Alaska to California) and L. ayresii (from British Columbia to California) together constituted a well-supported clade distinct from several genetically divergent Lampetra populations in Oregon and California, these two species were not reciprocally monophyletic. The genetically divergent populations included L. pacifica (from the Columbia River basin) and L. hubbsi (from the Kern River basin) and four Lampetra sp. populations in Oregon (Siuslaw River and Fourmile Creek) and California (Kelsey and Mark West Creeks). These four Lampetra sp. populations showed genetic divergence between 2.3 and 5.7% from any known species (and up to 8.0% from each other), and may represent morphologically cryptic and thus previously undescribed species. A fifth population (from Paynes Creek, California) may represent a range extension of L. hubbsi into the Upper Sacramento River.

Characterization of thirteen microsatellite markers in river and brook lampreys (Lampetra fluviatilis and L. planeri)

We describe the development based on 454 pyrosequencing technology of thirteen microsatellite markers for two closely related species of lamprey: Lampetra fluviatilis and L. planeri. The number of alleles per locus ranged from 2 to 5 in L. fluviatilis and from 2 to 6 in L. planeri. Gene diversity ranged from 0.062 to 0.718 in L. fluviatilis and from 0.322 to 0.677 in L. planeri. These markers will be helpful to study population genetic structure of both species and resolve their taxonomic status as separate species or ecotypes of a single species.

The effect of rapid and sustained decompression on barotrauma in juvenile brook lamprey and Pacific lamprey: Implications for passage at hydroelectric facilities

Fish passing downstream through hydroelectric facilities may pass through turbines where they experience a rapid decrease in pressure, which can lead to barotraumas including swim bladder rupture, exopthalmia, emboli, and hemorrhaging. In juvenile Chinook salmon, the main mechanism for injury is thought to be expansion of existing gases (particularly those present in the swim bladder) and the rupture of the swim bladder ultimately leading to exopthalmia, emboli and hemorrhaging. In fish lacking a swim bladder, such as lamprey, barotraumas due to rapid decompression may be reduced, however this has yet to be extensively studied. Another mechanism for barotrauma can be gases coming out of solution and the rate of this occurrence may vary among species. In this study, juvenile brook and Pacific lamprey acclimated to 146.2kPa (equivalent to a depth of 4.6m) were subjected to rapid (<1s) or sustained decompression (17min) to a very low pressure (13.8kPa) using a protocol previously applied to juvenile salmon. No mortality or evidence of barotraumas was observed following rapid decompression, nor up to 120h after sustained decompression. In contrast, mortality or injury would be expected for 97.5% of juvenile Chinook salmon exposed to a similar rapid decompression to these very low pressures. Additionally, juvenile Chinook salmon experiencing sustained decompression died within 7min. Thus, juvenile lamprey may not be susceptible to barotraumas associated with turbine passage to the same degree as juvenile salmonids.

Laboratory Testing of a Modified Electroshocking System Designed for Deepwater Juvenile Lamprey Sampling

AbstractA submersible sled with the ability to electroshock and detect larval lampreys via an optical camera was developed to sample deepwater rearing habitats (&gt;1 m). Three trials, each with 10 juvenile western brook lampreys Lampetra richardsoni (70–150 mm), were conducted in a laboratory setting to determine the effective shocking area and detection efficiency of the device. Electroshock was delivered for 30 s, and lamprey responses were observed. The detection efficiency ranged from 40% to 70% for the three trials (mean detection efficiency = 60%). Mean postshock emergence time was 4.4 s, and the maximum was 13 s. The device detected juvenile western brook lampreys without the need to transport them to the surface, thereby increasing sampling volume per unit time and reducing the potential for injury caused by handling. The system was developed to determine juvenile lamprey presence in regions where backpack electrofishers are unable to survey due to water depth.

Comparative Studies of Bile Acid Release in the Mature Male Lampreys

A comparative study of bile acid components from four lamprey species revealed that mature male chestnut lamprey Ichthyomyzon castaneus can produce 3 keto petromyzonol sulfate (3kPZS) while mature males of Pacific lamprey Lampetra tridentata, river lamprey Lampetra fluviatilis and American brook lamprey Lethenteron appendix produce petromyzonol sulfate (PZS). Identification of 3kPZS from a group of ancient lamprey species and of PZS from recently derived species led to a speculation that differentiation of bile acid biosynthetic systems has taken place during the course of evolution. Further studies on the biological functions of different bile acids in the adult lampreys are required to understand the evolution of chemical communication in lampreys.

Conflicting effects of woody debris on stream fish populations: implications for management

Summary1. Coarse woody debris (CWD) in stream channels causes changes in flow, sedimentation and ratios of pool to riffle areas. There is a consensus among fishery managers and scientists that CWD is beneficial to stream fish communities because of its enhancement of habitat diversity, invertebrate production and cover. Our hypothesis was that CWD accumulation or introduction would not increase in‐stream habitat capacity for all species and their ontogenic stages at reach and stream scales.2. The study used a system of gravel‐bed streams with naturally dynamic CWD accumulations and a fish community consisting of Salmo trutta, Cotttus gobio, Phoxinus phoxinus, Lampetra cf planeri, Nemacheilus barbatulus and Anguilla anguilla. Cotttus gobio and L. cf planeri are protected by an EU Directive and S. trutta is exploited for angling. Riffles, pools and CWD matrices, considered as the basic habitat/spatial units of channel structure, were sampled separately and abundance of each fish species quantified seasonally at each spatial scale.3. Multiple‐pass electric fishing techniques were used. Capture efficiencies were calculated for species, habitat and season. Areal densities (number m−2) were compared for habitat types and season using nonparametric anova. Canonical analysis and stepwise multiple regression were used to show the most influential physical variables on fish density. Densities were also compared by unit volume (numbers m−3) for pools and CWD matrices to investigate direct three‐dimensional use for cover. Reach‐scale densities for each fish species in relation to habitat composition were made using Spearman rank correlation of habitat‐scale densities with proportionate areas of the different habitat units in the reach.4. Habitat‐scale densities of bullheads and age 0+ trout were negatively correlated with depth and CWD areas for some seasons. Densities of lampreys, older trout, eels and minnows were positively correlated with depth in some seasons. Water depth had the most consistent influence on fish abundance at the habitat unit scale. Three‐dimensional comparisons of pools and CWD matrices indicated that only trout older than 1+ may use CWD habitats as cover.5. Reach‐scale densities of 0+ trout and bullheads were significantly correlated with proportion of riffle area and negatively with CWD and combined CWD‐pool habitat area in the reach. Densities of older trout, large eels and lampreys were positively correlated with CWD area and combined CWD‐pool area in some seasons. Inundation of riffles caused by impoundment upstream of CWD accumulations reduced spawning habitat for trout, bullheads, brook lampreys, minnows and stone loach. A trade‐off was an increase in refugia for older trout, minnows and eels.6. Coarse woody debris accumulation in streams is not beneficial to all species or ontogenic stages in a mixed species population and could severely limit essential habitat areas for some species. Thus, physical manipulation of channels should be implemented only after a thorough study of the habitat relationships of all species present, especially where protected species coexist with target species. The relative importance of in‐stream morphological changes depends on the spatial and temporal scale of the species life histories.

Contemporary gene flow between “paired” silver (Ichthyomyzon unicuspis) and northern brook (I. fossor) lampreys: implications for conservation

In most lamprey genera, “paired” species exist in which the larvae are morphologically similar or indistinguishable but, following metamorphosis, one species becomes parasitic while the other bypasses the adult feeding phase and rapidly becomes sexually mature. Since DNA barcoding and similar studies using short segments of the mitochondrial genome do not provide sufficient resolution to distinguish between recent divergence and a lack thereof, the current study examined the relationship between the parasitic silver lamprey (Ichthyomyzon unicuspis) and nonparasitic northern brook lamprey (I. fossor) using up to 10,230 bp from the mitochondrial genome to make phylogenetic inferences and mitochondrial restriction fragment length polymorphism (RFLP) and microsatellite markers to test for significant differences in allele frequencies. We found that silver and northern brook lampreys are not reciprocally monophyletic; two lineages were observed but each occurred within both species. There also were no significant range-wide differences in RFLP haplotype or microsatellite allele frequencies between the species, nor were there significant differences where they occurred sympatrically within the Lake Huron basin. Significant genetic differentiation was found only within the Lake Michigan basin where the results were potentially confounded by geographic separation. Our results thus support suggestions that silver and northern brook lampreys represent ecotypes of a single species since, where they are sympatric, they appear to be experiencing ongoing gene flow. However, alternative life history strategies can be important for a species’ long-term persistence, and critical data are needed to decide whether these two feeding types should be managed as a single unit.

Occurrence, abundance and biomass of fish in rivers of Latvia in accordance with river typology

This study analyses the structure of fish communities in 201 Latvian rivers: the number of species, their diversity, abundance and biomass of fish in accordance with the nationally accepted river typology and its parameters, i.e. the river basin area and the average slope. The number of species and their diversity as well as the abundance and biomass of fish vary significantly in rivers with different basin areas and temperature regimes. Latvian rivers can be classified into the following types based on the fish communities therein: (I) small coldwater rivers with trout and stone loach as dominant species, (II) small warmwater rivers dominated by stone loach, minnow, pike and perch, (III) medium coldwater rivers with such dominant species as brook lamprey, trout, minnow, stone loach and sculpin, (IV) medium warmwater rivers with pike, roach, gudgeon, minnow, stone loach and perch as dominant species, and (V) large potamal warmwater rivers dominated by pike, roach, chub, gudgeon, minnow, riffle minnow, ble...

Lampreys of the Iberian Peninsula: distribution, population status and conservation

The 3 lamprey species, sea lamprey Petromyzon marinus L., European river lamprey Lampetra fluviatilis L. and European brook lamprey L. planeri Bloch, that inhabit the Iberian Peninsula are of conservation concern. They are considered either Vulnerable, Critically Endan- gered, and even Extinct in different regions of this area mainly due to habitat loss and population fragmentation. Although several other factors contribute to the decline of lamprey populations in Iberian rivers, obstacles to migration (dams and weirs) are probably the most widespread and sig- nificant, causing an estimated 80% loss of accessible habitat in most river basins. We analysed his- torical records from all main Iberian rivers before the construction of impassable dams became widespread, and found that lampreys were consistently present in the upper reaches. The un - blocking of the lower stretches of major river basins and the restoration of former spawning sites and larval habitats should be considered as priority measures for the conservation of these spe- cies. Identification of Special Areas of Conservation to be included in the Natura 2000 European network can also be very relevant for lamprey conservation.

Fish Species of Greatest Conservation Need in Wadeable Iowa Streams: Current Status and Effectiveness of Aquatic Gap Program Distribution Models

AbstractEffective conservation of fish species of greatest conservation need (SGCN) requires an understanding of species–habitat relationships and distributional trends. Thus, modeling the distribution of fish species across large spatial scales may be a valuable tool for conservation planning. Our goals were to evaluate the status of 10 fish SGCN in wadeable Iowa streams and to test the effectiveness of Iowa Aquatic Gap Analysis Project (IAGAP) species distribution models. We sampled fish assemblages from 86 wadeable stream segments in the Mississippi River drainage of Iowa during 2009 and 2010 to provide contemporary, independent fish species presence–absence data. The frequencies of occurrence in stream segments where species were historically documented varied from 0.0% for redfin shiner Lythrurus umbratilis to 100.0% for American brook lamprey Lampetra appendix, with a mean of 53.0%, suggesting that the status of Iowa fish SGCN is highly variable. Cohen's kappa values and other model performance measures were calculated by comparing field‐collected presence–absence data with IAGAP model–predicted presences and absences for 12 fish SGCN. Kappa values varied from 0.00 to 0.50, with a mean of 0.15. The models only predicted the occurrences of banded darter Etheostoma zonale, southern redbelly dace Phoxinus erythrogaster, and longnose dace Rhinichthys cataractae more accurately than would be expected by chance. Overall, the accuracy of the twelve models was low, with a mean correct classification rate of 58.3%. Poor model performance probably reflects the difficulties associated with modeling the distribution of rare species and the inability of the large‐scale habitat variables used in IAGAP models to explain the variation in fish species occurrences. Our results highlight the importance of quantifying the confidence in species distribution model predictions with an independent data set and the need for long‐term monitoring to better understand the distributional trends and habitat associations of fish SGCN.Received April 16, 2011; accepted November 19, 2011