Distribution and habitat characteristics of Manayunkia speciosa and infection prevalence with the parasite Ceratomyxa shasta in the Klamath River, Oregon-California

A survey for Manayunkia speciosa, the freshwater polychaete host for the myxozoan parasite Ceratomyxa shasta, was conducted from 2003 to 2005 as part of an integrated study of the epizootiology of ceratomyxosis in Klamath River salmonids. Substrata samples (n = 257) were collected in a variety of habitats from Klamath Lake to the mouth of the Klamath River to document occurrence and relative abundance of the polychaete by habitat type and to estimate the prevalence of C. shasta within selected polychaete populations. Populations of M. specios a were identified throughout the Klamath River within pools (51.6%), eddy-pools (47.0%), and runs (40.0%). Large populations of M. speciosa were consistently found at the inflow to the main-stem reservoirs where densities were correlated with distance from the inflow into the reservoir. Using polymerase chain reaction assay and composite samples, 12 of 71 populations identified were tested for C. shasta, revealing a mean infection prevalence of 0.27%. An area of elevated infection prevalence (4.9 and 8.3%) was identified with 2 populations below a barrier to salmonid migration, which explains the high infectious spore densities demonstrated in concurrent studies and observations of C. shasta-induced mortality in Klamath River fall Chinook salmon (Oncorhynchus tshawytscha).     

Disparate infection patterns of Ceratomyxa shasta (Myxozoa) in rainbow trout (Oncorhynchus mykiss) and Chinook salmon (Oncorhynchus tshawytscha) correlate with internal transcribed spacer-1 sequence variation in the parasite

Ceratomyxa shasta is a virulent myxosporean parasite of salmon and trout in the Pacific Northwest of North America. The parasite is endemic in the Klamath River, Oregon/California, where a series of dams prevent movement of fish hosts between the upper and lower parts of the basin. Ceratomyxa shasta exhibits a range of infection patterns in different fish species above and below the dams. We hypothesised that the variations in infection and disease are indicators that different strains of the parasite exist, each with distinct host associations. Accordingly, we sought to identify strain-specific genetic markers in the ssrRNA and internal transcribed spacer region 1 (ITS-1). We examined 46 C. shasta isolates from water samples and two fish hosts, from June 2007 field exposures at upper and lower Klamath River sites with similarly high parasite densities. We found 100% of non-native rainbow trout became infected and died at both locations. In contrast, mortality in native Chinook salmon was <10% in the upper basin, compared with up to 40% in the lower basin. Parasite ssrRNA sequences were identical from all fish. However, ITS-1 sequences contained multiple polymorphic loci and a trinucleotide repeat (ATC)_0-3 from which we defined four genotypes: 0, I, II and III. Non-native rainbow trout at both sites were infected with genotype II and with a low level of genotype III. Chinook salmon in the upper basin had genotypes II and III, whereas in the lower basin genotype I predominated. Genotype I was not detected in water from the upper basin, a finding consistent with the lack of anadromous Chinook salmon there. Genotype O was only detected in water from the upper basin. Resolution of C. shasta into sympatric, host-specific genotypes has implications for taxonomy, monitoring and management of this significant parasite.     

Geographical and host distribution patterns of Parvicapsula minibicornis (Myxozoa) small subunit ribosomal RNA genetic types

Parvicapsula minibicornis is a myxozoan parasite implicated in mortalities of both juvenile and pre-spawning adult salmon in the Pacific Northwest of North America. Disease severity and presentation varies between salmon species and geographical localities. To better characterize population structure of the parasite, we sought genetic markers in the P. minibicornis ribosomal RNA gene. We compared samples from California with the type specimen from British Columbia, identified sequence variations, and then sequenced 197 samples from fish, river water and the parasite's polychaete worm host. Although DNA sequences of the parasite were >98·9% similar, there was enough variation to define 15 genotypes. All genotypes were detected in fish samples, although not in all species. A single genotype only was found in sockeye and pink salmon in the Fraser River Basin, but was not detected in sockeye from the adjacent Columbia River Basin. All coho salmon, irrespective of river basin, were infected with a unique mix of 2 genotypes. These data indicated that the P. minibicornis population exhibited strong signals of structuring by both geography and salmonid host species. Particular genotypes may correlate with disease differences seen in salmon populations in the Pacific Northwest.     

Distribution,prevalence and severity of Parvicapsula minibicornis infections among anadromous salmonids in the Fraser River,British Columbia,Canada

Polymerase chain reaction (PCR) and microscopic examination of stained kidney sections were used to diagnose infections with the myxozoan parasite Parvicapsula minibicornis in maturing Fraser River salmon. In 2 series of collections, the parasite was detected in 109 of 406 migrating sockeye salmon Oncorhynchus nerka belonging to Early Stuart, Early Summer and Summer run-timing groups, mainly upper Fraser River stocks. However, the parasite was detected neither in fish at sea nor once they had migrated several 100 km upstream. Prevalence then increased to 95% or greater at the spawning grounds. Histological examination of kidney was less sensitive than PCR in detecting the parasite in salmon collected from the earliest sites in both collections found positive by PCR. Severity of infection was greatest at the spawning grounds. Development of infection in sockeye, measured by prevalence, severity or by the rate of false-negative histological diagnoses, appeared to be a useful estimate of in-river residence time. Prevalence and severity of infections in sequential samples of Harrison River and Weaver Creek sockeye stocks collected from the Harrison River indicated that more time had elapsed since parasite transmission than would be predicted based on migration distance alone. Pink salmon Oncorhynchus gorbuscha, coho salmon O. kisutch and chinook salmon O. tshawytscha were found to be infected with the parasite. Development of P. minibicornis in pink salmon was most similar to that in sockeye. Pink and coho salmon may be at risk to the pathological consequences of P. minibicornis infection.     

Mortality threshold for juvenile Chinook salmon Oncorhynchus tshawytscha in an epidemiological model of Ceratomyxa shasta

The myxozoan parasite Ceratomyxa shasta is a significant pathogen of juvenile Chinook salmon Oncorhynchus tshawytscha in the Klamath River, California, USA. This parasite requires 2 hosts to complete its life cycle: a freshwater polychaete (Manayunkia speciosa) and a salmonid. The complex life cycle and large geographic area where infection occurs make it difficult to monitor and manage ceratomyxosis. We present a model for ceratomyxosis-induced mortality in O. tshawytscha, from which parameters important to the persistence of C. shasta are identified. We also experimentally quantify specific parameters from the model and identify a mortality threshold (a critical parameter), by naturally exposing native O. tshawytscha to C. shasta in the Klamath River. The average percent mortality that resulted from these experimental challenges ranged from 2.5 to 98.5% over an exposure dose of 4.4 to 612 x 10(6) parasites. This experiment identified a non-linear mortality threshold of 7.7 +/- 2.1 x 10(4) actinospores fish(-1) for Chinook salmon from the Iron Gate Hatchery on the Klamath River. Below this threshold no mortality occurred and above it mortality increased dramatically, thus providing a target by which to reduce parasitism in emigrating juvenile O. tshawytscha.     

Parvicapsula minibicornis in anadromous sockeye (Oncorhynchus nerka) and coho (Oncorhynchus kisutch) salmon from tributaries of the Columbia River

The myxosporean parasite Parvicapsula minibicornis is described from adult sockeye and coho salmon during spawning migrations in tributaries of the Columbia River in Canada and the United States. These observations extend the known distribution of this parasite from the Fraser River drainage basin. The parasite was identified in Columbia River salmonids using polymerase chain reaction (PCR) and by in situ hybridization, but unlike in Fraser River salmon, it was not observed in conventional histological preparations of the kidney. Prevalence of the parasite determined by PCR was higher in spawning sockeye from the Fraser River than in those from the Okanagan River. Our ability to explain the relatively low prevalence and absence of clinical P. minibicornis infections in Columbia River salmon is hampered by our poor understanding of the life cycle of this parasite.     

Density of the waterborne parasite Ceratomyxa shasta and its biological effects on salmon

The myxozoan parasite Ceratomyxa shasta is a significant pathogen of juvenile salmonids in the Pacific Northwest of North America and is limiting recovery of Chinook (Oncorhynchus tshawytscha) and coho (O. kisutch) salmon populations in the Klamath River. We conducted a 5-year monitoring program that comprised concurrent sentinel fish exposures and water sampling across 212 river kilometers of the Klamath River. We used percent mortality and degree-days to death to measure disease severity in fish. We analyzed water samples using quantitative PCR and Sanger sequencing, to determine total parasite density and relative abundance of C. shasta genotypes, which differ in their pathogenicity to salmonids. We detected the parasite throughout the study zone, but parasite density and genetic composition fluctuated spatially and temporally. Chinook and coho mortality increased with density of their specific parasite genotype, but mortality-density thresholds and time to death differed. A lethality threshold of 40% mortality was reached with 10 spores liter(-1) for Chinook but only 5 spores liter(-1) for coho. Parasite density did not affect degree-days to death for Chinook but was negatively correlated for coho, and there was wider variation among coho individuals. These differences likely reflect the different life histories and genetic heterogeneity of the salmon populations. Direct quantification of the density of host-specific parasite genotypes in water samples offers a management tool for predicting host population-level impacts.     

Involvement of Manayunkia speciosa (Annelida: Polychaeta: Sabellidae) in the life cycle of Parvicapsula minibicornis, a myxozoan parasite of Pacific salmon

A coelomic myxozoan infection was detected in freshwater polychaetes, Manayunkia speciosa from the Klamath River, Oregon/California, a site enzootic for the myxozoan parasites Ceratomyxa shasta and Parvicapsula minibicornis. The tetractinomyxon type actinospores had a near-spherical spore body 7.9 x 7.1 microm, with 3 spherical, protruding polar capsules, no valve cell processes, and a binucleate sporoplasm. Parvicapsula minibicornis-specific primers Parvi1f and Parvi2r amplified DNA from infected polychaetes in a polymerase chain reaction (PCR) assay. The small subunit 18S rRNA gene of the spores was sequenced (GenBank DQ231038) and was a 99.7% match with the sequence for P. minibicornis myxospore stage in GenBank (AF201375). Chinook salmon (Oncorhynchus tshawytscha) exposed to a dose of 1,000 actinospores per fish tested PCR positive for P. minibicornis at 14 wk postinfection and presporogonic stages were detected in the kidney tubules by histology at 20 wk. This life cycle is 1 of only about 30 known from more than 1,350 myxozoan species, and only the second known from a freshwater polychaete.     

Occurrence of the Myxosporidan Parasite Myxidium minteri in Salmonid Fish1

SYNOPSIS. The myxosporidan Myxidium minteri was found in 3 recognized hosts, chinook and coho salmon and rainbow trout and 2 new hosts, cutthroat trout and mountain whitefish. Spores in all species examined were found primarily in the gall bladder. Fish infected with this parasite were obtained from both Oregon coastal rivers and Columbia River basin locations. In general the prevalence of infection was higher in the fish in coastal rivers.     

Effects of host migration, diversity and aquaculture on sea lice threats to Pacific salmon populations

Animal migrations can affect disease dynamics. One consequence of migration common to marine fish and invertebrates is migratory allopatry-a period of spatial separation between adult and juvenile hosts, which is caused by host migration and which prevents parasite transmission from adult to juvenile hosts. We studied this characteristic for sea lice (Lepeophtheirus salmonis and Caligus clemensi) and pink salmon (Oncorhynchus gorbuscha) from one of the Canada's largest salmon stocks. Migratory allopatry protects juvenile salmon from L. salmonis for two to three months of early marine life (2-3% prevalence). In contrast, host diversity facilitates access for C. clemensi to juvenile salmon (8-20% prevalence) but infections appear ephemeral. Aquaculture can augment host abundance and diversity and increase parasite exposure of wild juvenile fish. An empirically parametrized model shows high sensitivity of salmon populations to increased L. salmonis exposure, predicting population collapse at one to five motile L. salmonis per juvenile pink salmon. These results characterize parasite threats of salmon aquaculture to wild salmon populations and show how host migration and diversity are important factors affecting parasite transmission in the oceans.     

Seasonal population dynamics of the nematode Cystidicoloides tenuissima (Zeder) from the River Swincombe, England

The seasonal population dynamics of adult and larval Cystidicoloides tenuissima were studied in its definitive hosts brown trout, Salmo trutta and juvenile Atlantic salmon, S. salar , and mayfly intermediate host, Leptophlebia marginata , from the River Swincombe, Dartmoor National Park, Devon, U.K. Infective larvae were present in each mayfly generation for almost its entire duration in the steam benthos. The infection parameters (prevalence and mean intensity) and maturation in the fish indicated C. tenuissima was an annual parasite exhibiting a seasonal periodicity and also systematic variation with the host age. Maturation was correlated to river water temperature. Infection parameters increased from September to May, then declined in June and July and remained relatively constant for the rest of the summer. Variation in the fish infection parameters over time, site, and host species appeared to be controlled by transmission related events; the availability of infective larvae, host feeding behaviour and water temperature. The availability of infective larvae and host diet controlled the rate at which parasites were added to the parasite population, but the pattern of gains and losses was determined by a temperature dependent rejection response.     

Molecular faunistics of accidental infections of <Emphasis Type="Italic">Gyrodactylus</Emphasis> Nordmann, 1832 (Monogenea) parasitic on salmon <Emphasis Type="Italic">Salmo salar</Emphasis> L. and brown trout <Emphasis Type="Italic">Salmo trutta</Emphasis> L. in NW Russia

Salmon Salmo salar L. and brown trout S. trutta L. juveniles were examined for the presence of accidental monogenean ectoparasitic species of Gyrodactylus Nordmann, 1832 in the Baltic and White Sea basins of Russian Karelia in order to estimate the frequency of host-switching attempts on an ecological timescale. To collect phylogeographical information and for exact species identification, the parasites were characterised by nuclear internal transcribed spacer sequences of rDNA (ITS) and, for some species, also by their mitochondrial DNA (CO1 gene) sequences. Four accidental Gyrodactylus species were observed on salmon and brown trout. A few specimens of G. aphyae Malmberg, 1957, the normal host of which is the Eurasian minnow Phoxinus phoxinus (L.), were observed on lake salmon from the Rivers Kurzhma (Lake Kuito, White Sea basin) and Vidlitsa (Lake Ladoga, Baltic basin). G. lucii Kulakovskaya, 1952, a parasite of the northern pike Esox lucius L., was observed on salmon in the Kurzhma. In the River Vidlitsa, two specimens of G. papernai Ergens & Bychowsky, 1967, normally on stone loach Barbatula barbatula (L.), were found on salmon. On anadromous White Sea salmon in the River Pulonga in Chupa Bay, a few salmon parr carried small colonies of G. arcuatus Bychowsky, 1933, which were shown to have originated from the local three-spined stickleback Gasterosteus aculeatus L. consumed as prey. No specimens of Gyrodactylus salaris Malmberg, 1957 were observed, although the Pulonga is the nearest salmon spawning river to the River Keret', which is heavily infected with introduced G. salaris. In the River Satulinoja, Lake Ladoga, three specimens of G. lotae Gusev, 1953, from burbot Lota lota (L.), were collected from a single brown trout S. trutta. All nonspecific gyrodactylid infections on salmonids were judged to be temporary, because only a few specimens were observed on each of the small number of infected fishes. The prevalence of endemic G. salaris was also low, only 1% (Nfish = 296) in Lake Onega and 0.7% (Nfish = 255) in Lake Ladoga, while brown trout specific Gyrodactylus species were not observed on any of the 429 trout examined from the Ladoga basin. The host-specific and unspecific burden of Gyrodactylus spp. on these 'glacial relict' populations of salmon and brown trout was very low, suggesting a generalised resistance against the co-evolved freshwater parasite community, or some kind of 'vaccination' effect. These hypotheses deserve further testing.     

Comparative susceptibility of brown trout and rainbow trout to Discocotyle sagittata (Monogenea)

The susceptibility of brown trout (Salmo trutta) and rainbow trout (Oncorhynchus mykiss) to the monogenean Discocotyle sagittata in the United Kingdom was assessed by experimental infection of naive fish. One month postinfection with 100 oncomiracidia/host, brown trout harbored significantly lower burdens (27.7 worms/host +/- 4.13 SE) than rainbow trout (47.8 worms/host +/- 3.90; P = 0.002). This indicates that the consistently lower prevalence and intensity of D. sagittata recorded in naturally infected farmed fishes reflects differences in susceptibility to the parasite. The outcome may be related to the comparatively short-term association of this parasite with rainbow trout (introduced to Britain in the 1880s) compared with the established native host-parasite association.     

Characterisation of a low pathogenic form of Gyrodactylus salaris from rainbow trout

Gyrodactylus salaris was isolated from rainbow trout in a Danish freshwater trout farm, and a laboratory population of this particular parasite form was established on rainbow trout. Challenge infections were performed using different salmonid strains and species, including East Atlantic salmon Salmo salar (from the Danish River Skjern?), Baltic salmon S. salar (from the Swedish River Ume Alv) and rainbow trout Oncorhynchus mykiss (from the Danish rainbow trout farm Fousing). These were compared to infection studies on the Norwegian Laerdalselva parasite form kept under exactly the same conditions in the laboratory. The Danish G. salaris form had low virulence towards both Atlantic and Baltic salmon, whereas rainbow trout proved susceptible to the parasite. The Danish G. salaris form was able to maintain a very low infection on East Atlantic salmon, but not on the Baltic salmon, which eliminated the infection within 2 wk. Rainbow trout developed infection intensities ranging up to several hundred parasites per host. The host colonization patterns of the parasite differed clearly from those of previous studies on microhabitats of the Norwegian form of G. salaris. A comparative study on morphological characters (opisthaptoral hard parts) from the Danish parasite form and Norwegian G. salaris showed no significant differences. Selected genes comprising internal transcribed spacers 1 and 2 (ITS), ribosomal RNA intergenic spacer (IGS) and cytochrome c oxidase subunit I (COI) regions were cloned and sequenced. Five sequenced ITS clones from 5 individuals of the Danish strain consistently revealed a single base substitution compared to ITS sequences from all other known species and strains of Gyrodactylus. Mitochondrial COI gene sequences demonstrated that the Danish G. salaris form is closely similar to the Laerdalselva parasite form found in Norway. The IGS sequences were highly variable, but very similar to those obtained from German isolates of G. salaris.     

Prevalence of Myxobolus cerebralis infections among genetic lineages of Tubifex tubifex at three locations in the Madison River, Montana

Host biodiversity can impact disease risk and influence the transmission of parasitic disease. Stream sediment-dwelling worms, Tubifex tubifex (Clitellata: Oligochaeta), are the definitive host of the parasite Myxobolus cerebralis (Myxozoa: Myxosporea), which causes whirling disease in salmonid fishes. Genetic diversity of T. tubifex is correlated with host susceptibility to M. cerebralis , and mitochondrial Lineage III is generally shown to be more likely to be infected and produce the triactinomyxon (TAM) spores than other lineages. We determined the mitochondrial lineage, relative abundance, and prevalence of infection of T. tubifex collected at 3 sites in the Madison River, Montana, where previous study had shown variation in whirling disease prevalence and severity in caged trout fry. We also compared visual identification of TAMs released from cultured worms with a molecular genetic assay (diagnostic polymerase chain reaction [PCR]) for parasite detection of both infected and uninfected worms. We estimated that mitochondrial Lineage III was most abundant at the site previously shown to have high fish disease and was also most likely to be infected. The 2 techniques for detecting parasite infection did not always agree, and the likelihood of PCR (+) and spore (-) was not significantly different from PCR (-) and spore (+). Differences in the relative infection prevalence for these 2 lineages may explain the wide range of infection in natural streams.     

Relationship between temperature and Ceratomyxa shasta -induced mortality in Klamath River salmonids

Water temperature influences almost every biological and physiological process of salmon, including disease resistance. In the Klamath River (California), current thermal conditions are considered sub-optimal for juvenile salmon. In addition to borderline temperatures, these fish must contend with the myxozoan parasite Ceratomyxa shasta , a significant cause of juvenile salmonid mortality in this system. This paper presents 2 studies, conducted from 2007 to 2010, that examine thermal effects on C. shasta -induced mortality in native Klamath River Chinook ( Oncorhynchus tshawytscha ) and coho ( Oncorhynchus kisutch ) salmon. In each study, fish were exposed to C. shasta in the Klamath River for 72 hr and then reared in the laboratory under temperature-controlled conditions. The first study analyzed data collected from a multi-year monitoring project to asses the influence of elevated temperatures on parasite-induced mortality during the spring/summer migration period. The second study compared disease progression in both species at 4 temperatures (13, 15, 18, and 21 C) representative of spring/summer migration conditions. Both studies demonstrated that elevated water temperatures consistently resulted in higher mortality and faster mean days to death. However, analysis of data from the multi-year monitoring showed that the magnitude of this effect varied among years and was more closely associated with parasite density than with temperature. Also, there was a difference in the timing of peak mortality between species; Chinook incurred high mortalities in 2008 and 2009, whereas coho was greatest in 2007 and 2008. As neither temperature nor parasite density can be easily manipulated, management strategies should focus on disrupting the overlap of this parasite and its obligate hosts to improve emigration success and survival of juvenile salmon in the Klamath River.     

Common sculpin Cottus gobio as a natural paratenic host of Proteocephalus longicollis (Cestoda: Proteocephalidae), a parasite of salmonids, in Europe.

Common sculpins Cottus gobio L. (Pisces: Cottidae), from the Mlynsky Brook near Ceské Zleby in the Sumava National Park, southwestern Bohemia, Czech Republic, were found to harbour in their intestines juvenile cestodes Proteocephalus longicollis (Zeder, 1800), a common parasite of holarctic salmonids, with a prevalence of 60% and intensity of 1 to 11 (mean 5) parasites per fish; undoubtedly, these prey fish serve as paratenic hosts. In this locality, the definitive host of P. longicollis is the brown trout Salmo trutta m. fario L., large specimens of which apparently acquire infection of this parasite by feeding on infected sculpins. C. gobio is the first known natural paratenic host of P. longicollis in Europe.     

Atlantic salmon (Salmo salar) and brown trout (Salmo trutta) differ in their suitability as hosts for the endangered freshwater pearl mussel (Margaritifera margaritifera) in northern Fennoscandian rivers

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Local patchiness of Gyrodactylus colemanensis and G. salmonis parasitizing salmonids in the South River watershed, Nova Scotia, Canada

Prevalence and intensity of Gyrodactylus colemanensis and G. salmonis (Monogenea) parasitizing juvenile/adult brook trout Salvelinus fontinalis, rainbow trout Oncorhynchus mykiss, brown trout Salmo trutta, and Atlantic salmon Salmo salar at 3 localities over an 8 km stretch in the South River, Nova Scotia, Canada, were calculated 4 times over a 9 mo period (October 2009, December 2009, March 2010, June 2010). G. colemanensis was on all 4 salmonids (endemic and non-endemic), while G. salmonis parasitized mostly S. fontinalis (endemic) and occasionally S. trutta (non-endemic). At an upstream locality, beyond a waterfall barrier, in a small tributary of the main river, G. colemanensis was more common than G. salmonis. In the main river, 7 km downstream, prevalence of G. colemanensis on S. fontinalis was comparable, or higher, than that of G. salmonis, while intensity of G. salmonis was higher than that of G. colemanensis. Downstream a further 1 km, in a tributary of the main river, both prevalence and intensity of G. salmonis on brook trout were higher than those of G. colemanensis. Stocks at a local trout hatchery had only G. colemanensis. The present study reports on a method by which exit water from such farms can be monitored for gyrodactylid parasites through a simple settling procedure. We estimated that up to 230,000 dislodged, live G. colemanensis exit the hatchery daily in discharge water entering the river. It is suggested that such systems are ideal for studying the impact of such parasite export on the nature of local parasite populations.     

Fragmentation of riverine systems: the genetic effects of dams on bull trout (Salvelinus confluentus) in the Clark Fork River system

Migratory bull trout (Salvelinus confluentus) historically spawned in tributaries of the Clark Fork River, Montana and inhabited Lake Pend Oreille as subadult and adult fish. However, in 1952 Cabinet Gorge Dam was constructed without fish passage facilities disrupting the connectivity of this system. Since the construction of this dam, bull trout populations in upstream tributaries have been in decline. Each year adult bull trout return to the base of Cabinet Gorge Dam when most migratory bull trout begin their spawning migration. However, the origin of these fish is uncertain. We used eight microsatellite loci to compare bull trout collected at the base of Cabinet Gorge Dam to fish sampled from both above and further downstream from the dam. Our data indicate that Cabinet Gorge bull trout are most likely individuals that hatched in above-dam tributaries, reared in Lake Pend Oreille, and could not return to their natal tributaries to spawn. This suggests that the risk of outbreeding depression associated with passing adults over dams in the Clark Fork system is minimal compared to the potential genetic and demographic benefits to populations located above the dams.