Relationship between Length of Roundtail Chub and Infection Intensity of Asian Fish Tapeworm Bothriocephalus acheilognathi

Abstract

Nonnative parasites have been blamed for the decline of native fish species in the American Southwest. The Asian fish tapeworm Bothriocephalus acheilognathi has parasitized many native fish species, but little is known of its effects on native cyprinid fish hosts. I found a strong negative correlation (Spearman's rank correlation, r_s = ?0.846; P < 0.001) between total length of roundtail chub Gila robusta and number of Asian fish tapeworms. A significant, but weaker negative correlation existed between weight of fish and number of tapeworms (r_s = ?0.687; P < 0.001). In addition, infected fish were significantly shorter (P = 0.0241) than uninfected fish. Infection by Asian fish tapeworm may slow growth, increase susceptibility to infestation, and increase predation on roundtail chub and possibly other native cyprinids.     

Recreational Angler Perspectives of Nonnative Fishes

Although fish invasions have implications for conservation and resource management, research on public attitudes toward nonnative fishes is lacking. We surveyed boat and canal bank recreational anglers in the Everglades to assess their awareness, preferences, and perspectives of native versus nonnative fishes. Our findings showed that 79% of anglers were aware of the presence of nonnative fishes, and overall awareness was positively affected by the frequency of fishing, and years of angler experience at study sites. Frequency of fishing had a stronger effect on canal bank anglers. Boat anglers had higher awareness of nonnatives, higher familiarity with “nonnative” terminology, and expressed greater preferences for native fish. Most anglers favored native species (72% preference), and targeted native fishes, particularly Florida Largemouth Bass (66%). Overall, findings show that despite the prevalence of nonnative species, anglers favored native fishes and supported native fish conservation.     

Spatial and temporal distribution of the Asian fish tapeworm Bothriocephalus acheilognathi (Cestoda: Bothriocephalidea) in the Rio Grande (Río Bravo del Norte)

Recent collections of the Asian fish tapeworm Bothriocephalus acheilognathi in the Rio Grande have raised concern about the potential impacts on Rio Grande endemic and imperiled fishes. The objectives of this study were to determine distribution and definitive hosts of the Asian fish tapeworm within the Rio Grande drainage and to quantify occurrences and abundances. In total, 1,992 fish spanning 11 families were collected and examined for Asian fish tapeworms in the Rio Grande and the Pecos and Devils rivers. The parasite was collected from red shiners Cyprinella lutrensis, Tamaulipas shiners Notropis braytoni, sand shiners N. stramineus, river carpsuckers Carpiodes carpio, plains killifish Fundulus zebrinus, western mosquitofish Gambusia affinis, blue suckers Cycleptus elongatus, blacktail shiners Cyprinella venusta, proserpine shiners Cyprinella proserpina, and Manantial roundnose minnow Dionda argentosa, with the latter four species being new host records. Monthly collections of red shiners from Big Bend National Park exhibited prevalence levels above 15% in January-March and December and below 10% during April-June and October. With over 50% of the Rio Grande icthyofauna in Texas considered imperiled, the occurrence and pathological effects of the Asian fish tapeworm in combination with reduced water quantity and quality and increased habitat fragmentation are of concern for these taxa.     

Predicted Redistribution of Ceratomyxa shasta Genotypes with Salmonid Passage in the Deschutes River,Oregon

Abstract

A series of dams on the Deschutes River, Oregon, act as migration barriers that segregate the river system into upper and lower basins. Proposed fish passage between basins would reunite populations of native potamodromous fish and allow anadromous fish of Deschutes River origin access to the upper basin. We assessed the potential redistribution of host-species-specific genotypes (O, I, II, III) of the myxozoan parasite Ceratomyxa shasta that could occur with fish passage and examined the influence of nonnative fish on genotype composition. To determine the present distribution of the parasite genotypes, we exposed eight salmonid species—three native and five stocked for sport fishing—in present and predicted anadromous salmonid habitats. We monitored fish for infection by C. shasta and sequenced a section of the parasite ribosomal DNA gene from fish and water samples to determine parasite genotype. Genotype O was present in both upper and lower basins and detected only in steelhead Oncorhynchus mykiss. Genotype I was spatially limited to the lower basin, isolated predominately from Chinook salmon O. tshawytscha, and lethal for this species only. Genotype II was detected in both basins and in multiple species, but only as a minor component of the infection. Genotype III was also present in both basins, had a wide host range, and caused mortality in native steelhead and multiple nonnative species. Atlantic salmon Salmo salar and kokanee O. nerka were the least susceptible to infection by any genotype of C. shasta. Our findings confirmed the host-specific patterns of C. shasta infections and indicated that passage of Chinook salmon would probably spread genotype I into the upper Deschutes River basin, but with little risk to native salmonid populations.

Received April 20, 2012; accepted July 19, 2012     

Aspects of the ecology of the Asian tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934 in yellowfish in the Vaal Dam, South Africa

Seasonal surveys were conducted at the Vaal Dam between April 2000 and January 2001. Twenty smallmouth yellowfish (Labeobarbus aeneus) and 20 largemouth yellowfish (Labeobarbus kimberleyensis) were collected with the aid of gill nets. Surface water quality variables were included. The cestodes were identified as either Bothriocephalus acheilognathi Yamaguti, 1934 or "other cestode spp.". The majority (99.8%) of the cestodes found in both yellowfish species were identified as B. acheilognathi (Asian tapeworm). The prevalence, mean intensity and abundance of B. acheilognathi in both yellowfish species were calculated. Ecological parameters including species specificity, seasonality, gender specificity and relationships between fish size and the Asian tapeworm prevalence were also included. In this study, B. acheilognathi preferred L. kimberleyensis over L. aeneus although a low intensity was observed in smallmouth yellowfish. Furthermore, the infection (in terms of prevalence, abundance and mean intensity) in largemouth yellowfish was markedly higher. Seasonal patterns observed in the Asian tapeworm's infection of smallmouth yellowfish are attributed to breeding and subsequent feeding patterns of this fish species with relatively high infections recorded in winter and spring. For L. kimberleyensis no explanation can be given regarding the seasonal patterns observed for the mean intensity and abundance of B. acheilognathi. The maximum and minimum mean intensity and abundance values in largemouth yellowfish were recorded in autumn and spring, respectively. In addition, the prevalence of B. acheilognathi was consistently high in all four seasons.     

Effectiveness of Praziquantel Bath Treatments against Bothriocephalus acheilognathi in Grass Carp

Abstract

Many states ban the importation of fish infected with the Asian tapeworm Bothriocephalus acheilognathi. Treatment with an effective tapeworm parasiticide prior to shipment would allow fish to be imported that might otherwise be rejected. In this study, extended praziquantel bath treatments of infected grass carp Ctenopharyngodon idella were tested to determine their efficacy against Asian tapeworms. Preliminary praziquantel treatments of 0.7 mg/L or more for an exposure period of 24 h at grass carp densities of 69 g/L were effective in eliminating all tapeworms from 22-g fish. When the treatment duration was lowered to 12 h, a praziquantel concentration of 2.8 mg/L was required for effective treatment. In replicated studies, significantly reduced tapeworm numbers (0–5 tapeworms per treated fish compared with 30+ tapeworms per control fish) were observed following 24-h exposures to praziquantel at 0.5, 0.7, 1.0, and 1.5 mg/ L. Tapeworm elimination occurred only at the maximum concentration of 1.5 mg/L when 88-g grass carp were stocked at a density of approximately 6 g/L. When fish density was raised to 60 g/L, the 1.5-mg/L treatment did not eliminate all tapeworms: 4 of 30 fish contained a single tapeworm.     

Production of Ceratonova shasta Myxospores from Salmon Carcasses: Carcass Removal Is Not a Viable Management Option

Severe infection by the endemic myxozoan parasite, Ceratonova (synonym, Ceratomyxa) shasta, has been associated with declines in and impaired recovery efforts of populations of fall-run Chinook Salmon Oncorhynchus tshawytscha in the Klamath River, California. The parasite has a complex life cycle involving a polychaete worm host as well as a salmon host. Myxospore transmission of this parasite, from salmon to polychaete, is a life cycle step during which there is a potential for applied disease management. A 3-year data set on prevalence, intensity, and spore characteristics of C. shasta myxospores was obtained from adult Chinook Salmon carcasses surveyed in the main stem of the Klamath River and three of its tributaries, Bogus Creek and the Shasta and Trinity rivers. Annual prevalence of myxospore detection in salmon intestines ranged from 22% to 52%, and spore concentration values per intestinal scraping ranged from 3.94 × 10² to 1.47 × 10⁷ spores. A prevalence of 7.3% of all carcasses examined produced >5.0 × 10⁵ spores, and these carcasses with “high” spore counts accounted for 76–95% of the total spores in a given spawning season. Molecular analysis of visually negative carcasses showed that 45–87% of these samples had parasite DNA, indicating they contained either low spore numbers or presporogonic stages of the parasite. Myxospores were rarely found in carcasses of freshly spawned adults but were common in decomposed carcasses of both sexes. The date of collection or age (based indirectly on FL) did not influence detection. The longer prespawn residence time for spring-run Chinook Salmon compared with that for fall-run Chinook Salmon in the Trinity River was associated with higher spore loads. The dye exclusion method for assessing spore viability in fresh smears indicated an inverse relationship in spore integrity and initial spore concentration. A carcass-removal pilot project in Bogus Creek for 6 weeks in the fall of 2008 (907 carcasses removed) and 2009 (1,799 carcasses removed) failed to measurably influence the DNA quantity of C. shasta in targeted waters. Combined with the high numbers of carcasses that contributed myxospores, we therefore deemed that this labor-intensive approach is not a viable management option to reduce the infectivity of C. shasta in Chinook Salmon in the Klamath River.

Received January 23, 2015; accepted September 28, 2015     

Interactions between bacteria and Cryptosporidium molnari in gilthead sea bream (Sparus aurata) under farm and laboratory conditions

The possible interaction of Cryptosporidium molnari and bacteria in gilthead sea bream (Sparus aurata) was studied. Epidemiological data from a pathological survey under farm conditions were analyzed. In addition, parasite and bacteria burdens were studied in experimental models in which naturally and experimentally parasitized fish were challenged with a particular strain of Vibrio harveyi (H57). All the bacteria species present were studied. Under farm conditions, the parasite was more prevalent when mortality or morbidity cases (study C) occurred than in randomly sampled fish (study B). In study C, parasite abundance was significantly higher in bacteria-negative fish, and total bacteria abundance was significantly higher within non-parasitized fish. V. harveyi and V. splendidus were the most prevalent among bacteria carriers in studies B and C, respectively. In study C, among bacteria carriers, most isolates were slightly more prevalent in parasitized than in non-parasitized fish. Two groups (G1, G2) of naturally parasitized fish were inoculated with H57 by intracoelomic injection (ICI) and by oral intubation (OI). H57 was recovered only in G1 inoculated fish, which had a significantly higher basal abundance of total bacteria, and where the only ones with mortalities. In G1, the mortality rate and the prevalence of other V. harveyi strains different from the H57 molecular type were higher in ICI than in OI fish, and the total bacteria abundance was also significantly higher in ICI fish. C. molnari abundance was significantly higher in G1 than in G2, and also in OI than in ICI fish within G1. When H57 was IC inoculated to fish (G3, from the same farm as G2) experimentally infected with C. molnari, H57 was not recovered from any fish. A low mortality was recorded, and only in those fish inoculated with both pathogens. Also in these fish, the prevalence of infection of C. molnari was higher and histopathological damage to the stomach was greater than in fish inoculated only with the parasite. Therefore, the impact of the parasite would be reduced notably when the bacterial burden or the intensity of parasite infection are low (G2, G3).     

Absence of a Grass/Fire Cycle in a Semiarid Grassland: Response to Prescribed Fire and Grazing

Many nonnative invasive grasses alter fire regimes to their own benefit and the detriment of native organisms. In southern Arizona the nonnative Lehmann lovegrass (Eragrostis lehmanniana Nees) dominates many semiarid grasslands where native grasses were abundant. Managers are wary of using prescribed fire in this fire-prone community partly due to the perceived effects of a grass/fire cycle. However, examples of the grass/fire cycle originate in ecosystems where native plants are less fire-tolerant than grasses and the invasive plant does not mimic the physiognomy of the native community. We investigate the effects of prescribed fire and livestock grazing on a semiarid grassland community dominated by a nonnative invasive grass. Lehmann lovegrass does not appear to alter the fire regime of semiarid grasslands to the detriment of native plants. Prescribed fire reduced the abundance of Lehmann lovegrass for 1 to 2 yr while increasing abundance of native grasses, herbaceous dicotyledons and fall richness, and diversity. Effects of livestock grazing were less transformative than the effects of fire in this long-grazed area, but grazing negatively affected native plants as did the combination of prescribed fire and livestock grazing. Although Lehmann lovegrass produces more fuel than native plants, fire frequency in semiarid grasslands appears to be limited by the paucity of above-average precipitation, which constrains high fuel loads. In addition, many native grasses tolerate high temperatures produced by Lehmann lovegrass fires. Consistent with previous research, fire does not promote the spread of Lehmann lovegrass, and more importantly human alteration of the fire regime is greater than the nominal effects of Lehmann lovegrass introduction on the fire regime.     

First record of Bothriocephalus acheilognathi in the Rio Grande with comparative analysis of ITS2 and V4-18S rRNA gene sequences

Bothriocephalus acheilognathi is an introduced tapeworm in North America often reported as a serious ecological threat to native fishes. In this paper, we report the first record of B. acheilognathi in the Big Bend region of the Rio Grande in Texas (known as the Río Bravo del Norte in Mexico). Identification of B. acheilognathi was confirmed by morphologic and genetic techniques (sequences of ITS2 and V4-18S rRNA genes). Its prevalence was 27% and its intensity ranged from 1 to 5 individuals in a January 2006 collection of 115 red shiners Cyprinella lutrensis. In addition, it was found in the Tamaulipas shiner Notropis braytoni, a Rio Grande endemic and a new host record. The occurrence of B. acheilognathi might have negative ecological impacts on endemic fishes in the Rio Grande. Several of the fishes that could serve as definitive hosts are of conservation concern. Its occurrence also might affect the success of reintroducing the Rio Grande silvery minnow Hybognathus amarus, which is federally listed as endangered, in this portion of the Rio Grande.     

Baiting intervals and duration of control of the small fox tapeworm: a simulation study

Field trials to control the small fox tapeworm Echinococcus multilocularis failed to reduce the prevalence of the parasite persistently. With the experience from this empirical work, a simulation model for the population dynamics of the small fox tapeworm was developed. This model is used to examine the effect of different control strategies. Sufficient control duration is able to eradicate the parasite in simulation experiments. Baiting intervals of 4 or 6 weeks were found to be more efficient than shorter or longer intervals. The strategy used in field trials showed no sustainable effect in any of the simulation experiments. The applicability of simulation models for the planning of control measures for wildlife diseases is discussed.     

Squash-Plate Technique for Detecting Asian Tapeworms in Fish

Abstract

A method for detecting the Asian tapeworm Bothriocephalus acheilognathi in fish is described. Glass slides or plates are used to flatten the intestinal tract, and the worms are detected by reflected light and low-power microscopy.     

Comparative susceptibility of Deschutes River, Oregon, Tubifex tubifex populations to Myxobolus cerebralis

Dams along the Deschutes River (DR) in central Oregon have blocked fish migration for over 40 years. Reestablishment of anadromous fish runs above the dams as part of a fish passage plan may introduce fish pathogens, such as Myxobolus cerebralis, the myxozoan parasite that causes salmonid whirling disease. This parasite is carried by adult salmon that stray into the DR system during their return to enzootic areas of the upper Columbia River basin, and it is now known to be established in at least one lower DR tributary. The life cycle of M. cerebralis involves two obligate hosts: a salmonid and the oligochaete worm Tubifex tubifex. To determine the likelihood of parasite establishment above the DR dams, we conducted benthic sediment surveys between 1999 and 2007 and found that T. tubifex had a patchy distribution and low relative abundance. Mitochondrial 16S ribosomal DNA gene analysis indicated that two lineages of T. tubifex (III and VI) were present both above and below the dams. Laboratory susceptibility studies to characterize differences in infection prevalence and parasite production between nine T. tubifex populations revealed that production varied considerably among exposed groups and was proportional to the number of lineage III worms present. Our results suggest that M. cerebralis could become established above the dams if infected fish are allowed passage into the upper DR system, but not all areas of the DR basin can be classified as having the same likelihood for parasite establishment, and the potential impact will be location dependent.     

Differing Resistance of Atlantic Salmon Strains and Rainbow Trout to Gyrodactylus salaris Infection

Abstract

Laboratory studies were conducted on the susceptibility of different strains of Atlantic salmon Salmo salar and rainbow trout Oncorhynchus mykiss to infection with the monogenean Gyrodactylus salaris. This parasite, probably originating from the Baltic Sea region, is known to minimally affect Neva River (Baltic Sea) Atlantic salmon. However, following its introduction into Norway, G. salaris has caused severe mortality and morbidity among Norwegian Atlantic salmon, which are considered a highly susceptible strain. The cohabitation experiment included one stock of rainbow trout and four different strains of Atlantic salmon from the Baltic Sea region (Mörrum River, Sweden), Europe (Skjern River, Denmark; Conon River, Scotland), and North America (Bristol Cove River, Canada). Fish were exposed to a Norwegian strain of G. salaris, and parasite population development and distribution were monitored for 7 weeks. Rainbow trout exhibited low susceptibility to G. salaris infection, whereas Conon River and Skjern River Atlantic salmon were highly susceptible and exhibited high mortality rates. Mörrum River Atlantic salmon exhibited intermediate susceptibility and low mortality. Bristol Cove River Atlantic salmon harbored relatively low parasite numbers, but fish mortality was high. Our experiment showed that the Danish Skjern River strain of Atlantic salmon is highly susceptible to G. salaris infection, further supporting the hypothesis that Atlantic Ocean strains are more susceptible to G. salaris infection than are Baltic strains.     

Introduction,establishment and spread of the Southern mouthbrooder Pseudocrenilabrus philander in the Baakens River,Eastern Cape,South Africa

This paper provides evidence for the extralimital establishment and spread of Pseudocrenilabrus philander in the Baakens River, Eastern Cape, South Africa. Since the first occurrence record at a single locality in 1994 this species has now spread throughout the river and the population contains both reproductive adults and juveniles. Gut content analysis demonstrated potential dietary overlap with native fishes and predation on fish larvae. Pseudocrenilabrus philander in the Baakens River therefore satisfies all criteria for an invasive species in this river and was categorised as invasive using a unified framework for biological invasions.     

First Record of Bothriocephalus acheilognathi in the Rio Grande with Comparative Analysis of ITS2 and V4-18S rRNA Gene Sequences

Abstract

Bothriocephalus acheilognathi is an introduced tapeworm in North America often reported as a serious ecological threat to native fishes. In this paper, we report the first record of B. acheilognathi in the Big Bend region of the Rio Grande in Texas (known as the Río Bravo del Norte in Mexico). Identification of B. acheilognathi was confirmed by morphologic and genetic techniques (sequences of ITS2 and V4-18S rRNA genes). Its prevalence was 27% and its intensity ranged from 1 to 5 individuals in a January 2006 collection of 115 red shiners Cyprinella lutrensis. In addition, it was found in the Tamaulipas shiner Notropis braytoni, a Rio Grande endemic and a new host record. The occurrence of B. acheilognathi might have negative ecological impacts on endemic fishes in the Rio Grande. Several of the fishes that could serve as definitive hosts are of conservation concern. Its occurrence also might affect the success of reintroducing the Rio Grande silvery minnow Hybognathus amarus, which is federally listed as endangered, in this portion of the Rio Grande.     

Investigation on Opisthorchis felineus occurrence and life cycle in Italy

Opisthorchiasis is a fish borne parasitic infection caused by helminths of the genus Opisthorchis (Digenea, Opisthorchiidae), affecting humans and other fish-eating mammals. Despite Opisthorchis felineus was first described in Italy in 1884, no cases of human opisthorchiasis were reported in this country until 2004; from then on, 4 outbreaks due to this species have been recorded in Central Italy. Following the more relevant of these outbreaks, involving 34 people in August 2007, snails, fishes and fecal samples collected from the Bolsena and Bracciano lakes (Central Italy) were analyzed in order to define the cycle of O. felineus in the area and investigate its prevalence in the different hosts. Pools of 20-40 snails each (4983 specimens altogether) of the genus Bithynia were analyzed by PCR for parasite DNA detection. Eight hundred and ninety-four fish belonging to 12 species were collected from the two lakes and tested for metacercariae both by muscle compression and digestion techniques. Eighty-seven fecal samples of 5 putative definitive host species were collected very close to the two lakes and tested for parasite eggs detection by formalin-ethyl acetate concentration technique. Identification at the species level of metacercariae and eggs, respectively, from fish and stool was confirmed by PCR analysis and sequencing. O. felineus DNA was detected in 0.08% (overall minimum infection rate) of snails of the genus Bithynia from the two lakes. The tench, Tinca tinca, was the only fish found infested in both lakes (prevalence 88.5%). O. felineus eggs were found only in cat feces (prevalence 46.4%). The tench represents the only threat for the human consumption in the study area while Coregonus sp., the most economically important species for the local fishery and frequently consumed raw marinated, resulted to be not infected. The high prevalence recorded both in fish and in definitive host suggests a widespread and massive presence of the parasite in the area. Further studies are needed to better investigate the possible role of some cyprinids species as intermediate hosts, in order to check their safety for human consumption.     

Metacercarial distribution of Centrocestus formosanus among fish hosts in the Guadalupe River drainage of Texas

We examined the gills of wild fish collected from central Texas for Centrocestus formosanus metacercariae to determine whether this temperature-restricted parasite had invaded the thermally dynamic Guadalupe River via an introduced population in its thermally stable tributary, the Comal River. We collected fish from three sites in the Guadalupe River near its confluence with the Comal River (upstream, at, and downstream) and one site in the Comal River. Centrocestus formosanus infected 14 of the 25 species examined (56.0%) and 171 of the individual fish (27.1%). Several of the infected fish represent new host records for the parasite, and two are listed as species of special concern by the state of Texas. Mean metacercarial intensities varied from 8 to 616 among species, and the highest recorded intensity was greater than 800 in two Guadalupe roundnose minnow Dionda nigrotaeniata. Among the 24 species examined from the Guadalupe River, 11 (45.8%) were infected with C. formosanus. Thorough surveys at the study sites yielded no living specimens of the first obligate intermediate snail host (red-rim melania Melanoides tuberculatus), which must be present to perpetuate the parasite. Thus, the infections were probably due to drifting cercariae that had been shed into the water column upstream of the study area in the Comal River. We therefore investigated spatial patterns in cercarial acquisition using caged fish to determine whether drifting cercariae were present in the water column at the study sites. Of 57 uninfected blacktail shiners Cyprinella venusta exposed to Guadalupe River water downstream from and at the confluence, 52 (91.2%) became infected with C. Formosanus metacercariae at a mean rate of 4 metacercariae/d. This finding extends the known geographic range of this invasive exotic parasite and is the first report of the life cycle being advanced in the fish assemblage of a thermally variable temperate stream in the USA.     

Zoonotic diseases of fish and their prevention and control

Fish and aquatic-derived zoonotic diseases have caused considerable problems in the aquaculture industry and fishery worldwide. In particular, zoonotic diseases can pose widespread threats to humans. With the world’s growing population and potential global trade of aquaculture and fish, the risk of environmental contamination and development of fish and aquatic-derived zoonoses in humans are increasing. The important causes of zoonoses include bacteria, parasites, viruses, and fungi. The zoonotic bacterial agents are divided into two main groups: Gram-positive (Mycobacteriaceae, Streptococcaceae, Erysipelothricaceae families) and Gram-negative (Aeromonadaceae, Vibrionaceae, Pseudomondaceae, Enterobacteriaceae, and Hafniaceae families). The premier parasitic agents include cestodes (tapeworm; e.g. Diphyllobothrium spp.), trematodes (fluke; e.g. Opisthorchis spp.), and nematodes (round worm; e.g. Anisakis spp.). In addition, protozoan organisms such as Cryptosporidium spp. are also considered fish-derived zoonotic pathogens. Two groups of fish-associated fungi causing basidiobolomycosis and sporotrichosis also pose a zoonotic risk for humans. The majority of the fish-derived zoonotic diseases are transmitted to humans mainly via the consumption of improperly cooked or raw fish or fish products. Therefore, the incidence of zoonotic diseases can be reduced by properly processing fish and fish products, e.g. by thermal (heat/freezing) treatment. The prevalence of zoonotic agents in fishes varies seasonally and should be regularly monitored to evaluate the prevalence of pathogens in both wild and cultured fish populations. This review focuses on the fish zoonotic agents/diseases and their control and prevention.