Ecological inferences on invasive carp survival using hydrodynamics and egg drift models.

Bighead carp (Hypophthalmichthys nobilis), silver carp (H. molitrix), black carp (Mylopharyngodon piceus), and grass carp (Ctenopharyngodon idella), are invasive species in North America. However, they hold significant economic importance as food sources in China. The drifting stage of carp eggs has received great attention because egg survival rate is strongly affected by river hydrodynamics. In this study, we explored egg-drift dynamics using computational fluid dynamics (CFD) models to infer potential egg settling zones based on mechanistic criteria from simulated turbulence in the Lower Missouri River. Using an 8-km reach, we simulated flow characteristics with four different discharges, representing 45-3% daily flow exceedance. The CFD results elucidate the highly heterogeneous spatial distribution of flow velocity, flow depth, turbulence kinetic energy (TKE), and the dissipation rate of TKE. The river hydrodynamics were used to determine potential egg settling zones using criteria based on shear velocity, vertical turbulence intensity, and Rouse number. Importantly, we examined the difference between hydrodynamic-inferred settling zones and settling zones predicted using an egg-drift transport model. The results indicate that hydrodynamic inference is useful in determining the 'potential' of egg settling, however, egg drifting paths should be taken into account to improve prediction. Our simulation results also indicate that the river turbulence does not surpass the laboratory-identified threshold to pose a threat to carp eggs.

Movement ecology of diploid and triploid grass carp in a large reservoir and upstream tributaries.

Grass carp Ctenopharyngodon idella, is an herbivorous fish originally brought to North America from Asia in 1963 to control nuisance aquatic vegetation. Since their arrival, detrimental alterations to aquatic ecosystems have sometimes occurred in waterways where they were initially stocked and into which they have escaped. The movements of grass carp from lentic systems into tributaries required for spawning is poorly understood, and understanding environmental conditions associated with upstream migrations may aid in management of the species. We stocked 43 fertile diploid and 43 sterile triploid grass carp implanted with acoustic transmitters into Truman Reservoir, Missouri, USA between January 2017 and October 2018 to characterize movements during spring and summer when spawning conditions occur. Twenty fish (11 diploid/9 triploid) exhibited upstream migration behavior in the Osage River, a major tributary, in 2018 and 2019. Migration primarily occurred in April and May, during high discharge events associated with increasing river stage when water temperatures were between 15 and 28°C. Observed migrations ranged from 3.0-108 river km in length, and six individuals were observed making multiple upstream migrations in one season. Eleven fish initiated upstream migrations while in the lentic main body of the reservoir. These findings provide some evidence for upstream migrations by diploid and triploid grass carp as well both lake and river residents. Evidence of similar upstream migration behavior by both diploid and triploid grass carp suggests that triploids may be suitable surrogates for diploids for study of movement ecology. Removal efforts in tributaries targeting periods of increasing river stage during spring may provide the best opportunity of encountering large concentrations of grass carp.

Developmental ecomorphology of the epibranchial organ of the silver carp, Hypophthalmichthys molitrix.

Silver carp regularly consume and digest particles of food as small as 5 µm. This ability drives their efficient consumption of phytoplankton and because they feed low on the food chain they have an important place in aquaculture worldwide. In North America, where they are considered invasive, silver carp deplete food resources for native species and in so doing occupy increased niche space. Here, we determine the ontogenetic stage and size at which silver carp are morphologically capable of primarily feeding on particles <10 µm. Ecological studies on this species have shown that there is an ontogenetic shift in diet as predominantly zooplanktivorous juveniles later switch to eating much smaller phytoplankton. The occupation of this new trophic niche presents both a metabolic and a mechanical challenge to these fish, since it is unclear how they can efficiently feed on such small particles. We hypothesize that the epibranchial organ (EBO) in silver carp is essential in aggregating these small particles of food, allowing the species to consume mass quantities of tiny particles, thus mitigating metabolic constraints. In this study, we investigate early ontogeny of the EBO in silver carp to determine when this structure achieves the requisite morphology to become functional. We find that at around 80 mm standard length (SL) the EBOs are consistently filled with food, demonstrating that this accumulating organ has become functional. This size corresponds with previous ecological data documenting important shifts in the type of food consumed. While the basic bauplan of the EBO is established very early in ontogeny (by 15 mm SL), multiple waves of histological maturation of muscle, cartilage, gill rakers and epithelium ultimately form the functional structure.

Could a freshwater fish be at the root of dystrophic crises in a coastal lagoon?

Eutrophication has a profound impact on ecosystems worldwide. Grass carp Ctenopharyngodon idella, an herbivorous fish, has been introduced to control aquatic plant overgrowth caused by eutrophication, but could have other, potentially detrimental, effects. We used the Po di Volano basin (south of the Po River delta, northern Italy) as a test case to explore whether grass carp effects on canal aquatic vegetation could be at the root of historical changes in N loads exported from the basin to the Goro Lagoon. We modeled the aquatic vegetation production and standing crop, its denitrification potential, and its consumption by introduced grass carp. We then examined whether changes in historical nitrogen loads matched the modeled losses of the drainage network denitrification function or other changes in agricultural practices. Our results indicate that introduced grass carp could completely remove submerged vegetation in the Po di Volano canal network, which could - in turn - lead to substantial loss of the denitrification function of the system, causing in an increase in downstream nitrogen loads. A corresponding increase, matching both timing and magnitude, was detected in historical nitrogen loads to the Goro Lagoon, which were significantly different before and after the time of modeled collapse of the denitrification function. This increase was not clearly linked to watershed use or agricultural practices, which implies that the loss of the denitrification function through grass carp overgrazing could be a likely explanation of the increase in downstream nitrogen loads. Perhaps for the first time, we provide evidence that a freshwater fish introduction could have caused long-lasting changes in nutrient dynamics that are exported downstream to areas where the fish is not present.

Survival and drifting patterns of grass carp eggs and larvae in response to interactions with flow and sediment in a laboratory flume.

A series of laboratory experiments was conducted to better understand the behavior of grass carp eggs and larvae in moving water in order to develop and implement new strategies for control and prediction of their dispersal and drift at early life stages. Settling velocity and density of a representative sample of eggs were estimated, and three trials of flume experiments with different flow conditions were conducted with live eggs in a temperature-controlled setting with a mobile sediment bed. In these trials, egg and larval stages were continuously analyzed over periods of 80 hours; and eggs and larvae interactions with the flow and sediment bed were monitored and characterized qualitatively and quantitatively. Survival rates were quantified after each trial, highlighting physical causes for increased mortality. Detailed flow analysis was correlated to the observed drifting and swimming behavior of eggs and larvae, to estimate distributions across the water depth, as well as traveling and swimming speeds. Evidence of the influence of mean and turbulent flow in the suspension and transport of eggs are reported, and swimming patterns of larvae at different developmental stages are described. These findings support the development of new strategies for monitoring the spread of grass carp eggs and larvae in rivers, and provide new inputs to predict conditions favorable for spawning and hatching, allowing for mitigation measures at early life stages, which are critical to control their dispersal.

Ontogenetic changes in swimming speed of silver carp, bighead carp, and grass carp larvae: implications for larval dispersal.

Bighead, silver, and grass carps are invasive in the waterways of central North America, and grass carp reproduction in tributaries of the Great Lakes has now been documented. Questions about recruitment potential motivate a need for accurate models of egg and larval dispersal. Quantitative data on swimming behaviors and capabilities during early ontogeny are needed to improve these dispersal models. We measured ontogenetic changes in routine and maximum swimming speeds of bighead, grass, and silver carp larvae. Daily measurements of routine swimming speed were taken for two weeks post-hatch using a still camera and the LARVEL program, a custom image-analysis software. Larval swimming speed was calculated using larval locations in subsequent image frames and time between images. Using an endurance chamber, we determined the maximum swimming speed of larvae (post-gas bladder inflation) for four to eight weeks post-hatch. For all species, larval swimming speeds showed similar trends with respect to ontogeny: increases in maximum speed, and decreases in routine speed. Maximum speeds of bighead and grass carp larvae were similar and generally faster than silver carp larvae. Routine swimming speeds of all larvae were highest before gas bladder inflation, most likely because gas bladder inflation allowed the fish to maintain position without swimming. Downward vertical velocities of pre-gas bladder inflation fish were faster than upward velocities. Among the three species, grass carp larvae had the highest swimming speeds in the pre-gas bladder inflation period, and the lowest speeds in the post-gas bladder inflation period. Knowledge of swimming capability of these species, along with hydraulic characteristics of a river, enables further refinement of models of embryonic and larval drift.

Correction: Isotope niche dimension and trophic overlap between bigheaded carps and native filter-feeding fish in the lower Missouri River, USA.

[This corrects the article DOI: 10.1371/journal.pone.0197584.].

Isotope niche dimension and trophic overlap between bigheaded carps and native filter-feeding fish in the lower Missouri River, USA.

Stable carbon and nitrogen isotope values (δ13C and δ15N) were used to evaluate trophic niche overlap between two filter-feeding fishes (known together as bigheaded carp) native to China, silver carp (Hypophthalmichthys molitrix) and bighead carp (Hypophthalmichthys nobilis), and three native filter-feeding fish including bigmouth buffalo (Ictiobus cyprinellus), gizzard shad (Dorosoma cepedianum) and paddlefish (Polyodon spathula) in the lower Missouri River, USA, using the Bayesian Stable Isotope in R statistics. Results indicate that except for bigmouth buffalo, all species displayed similar trophic niche size and trophic diversity. Bigmouth buffalo occupied a small trophic niche and had the greatest trophic overlap with silver carp (93.6%) and bighead carp (94.1%) followed by gizzard shad (91.0%). Paddlefish had a trophic niche which relied on some resources different from those used by other species, and therefore had the lowest trophic overlap with bigheaded carp and other two native fish. The trophic overlap by bigheaded carp onto native fish was typically stronger than the reverse effects from native fish. Average niche overlap between silver carp and native species was as high as 71%, greater than niche overlap between bighead carp and native fish (64%). Our findings indicate that bigheaded carps are a potential threat to a diverse and stable native fish community.

First evidence of bighead carp wild recruitment in Western Europe, and its relation to hydrology and temperature.

Bighead carp (Hypophthalmichthys nobilis) have been introduced throughout Europe, mostly unintentionally, and little attention has been given to their potential for natural reproduction. We investigated the presence of young-of-the-year bighead carp in an irrigation canal network of Northern Italy and the environmental conditions associated with spawning in 2011-2015. The adult bighead carp population of the canal network was composed by large, likely mature, individuals with an average density of 45.2 kg/ha (over 10 fold more than in the main river). The 29 juvenile bighead carp found were 7.4-13.1 cm long (TL) and weighed 9.5-12.7 g. Using otolith-derived spawning dates we estimated that these juveniles were 94-100 days old, placing their fertilization and hatch dates in mid-to-end-June. Using this information in combination with thermal and hydraulic data, we examined the validity of existing models predicting the onset of spawning conditions and the viability of egg pathways to elucidate spawning location of the species. While evidence of reproduction was not found every year, we determined that potentially viable spawning conditions (annual degree-days and temperature thresholds) and pathways of egg drift suitable for hatching are present in short, slow-flowing canals.

Embryonic and larval development and early behavior in grass carp, Ctenopharyngodon idella: implications for recruitment in rivers.

With recent findings of grass carp Ctenopharyngodon idella in tributaries of the Great Lakes, information on developmental rate and larval behavior is critical to efforts to assess the potential for establishment within the tributaries of that region. In laboratory experiments, grass carp were spawned and eggs and larvae reared at two temperature treatments, one "cold" and one "warm", and tracked for developmental rate, egg size, and behavior. Developmental rate was quantified using Yi's (1988) developmental stages and the cumulative thermal units method. Grass carp had a thermal minimum of 13.5°C for embryonic stages and 13.3°C for larval stages. Egg size was related to temperature and maternal size, with the largest eggs coming from the largest females, and eggs were generally larger in warmer treatments. Young grass carp larvae exhibited upward and downward swimming interspersed with long periods of lying on the bottom. Swimming capacity increased with ontogeny, and larvae were capable of horizontal swimming and position holding with gas bladder emergence. Developmental rates, behavior, and egg attributes can be used in combination with physical parameters of a river to assess the risk that grass carp are capable of reproduction and recruitment in rivers.

Fish gut microbiota analysis differentiates physiology and behavior of invasive Asian carp and indigenous American fish.

Gut microbiota of invasive Asian silver carp (SVCP) and indigenous planktivorous gizzard shad (GZSD) in Mississippi river basin were compared using 16S rRNA gene pyrosequencing. Analysis of more than 440 000 quality-filtered sequences obtained from the foregut and hindgut of GZSD and SVCP revealed high microbial diversity in these samples. GZSD hindgut (GZSD_H) samples (n=23) with >7000 operational taxonomy units (OTUs) exhibited the highest alpha-diversity indices followed by SVCP foregut (n=15), GZSD foregut (n=9) and SVCP hindgut (SVCP_H) (n=24). UniFrac distance-based non-metric multidimensional scaling (NMDS) analysis showed that the microbiota of GZSD_H and SVCP_H were clearly separated into two clusters: samples in the GZSD cluster were observed to vary by sampling location and samples in the SVCP cluster by sampling date. NMDS further revealed distinct microbial community between foregut to hindgut for individual GZSD and SVCP. Cyanobacteria, Proteobacteria, Actinobacteria and Bacteroidetes were detected as the predominant phyla regardless of fish or gut type. The high abundance of Cyanobacteria observed was possibly supported by their role as the fish's major food source. Furthermore, unique and shared OTUs and OTUs in each gut type were identified, three OTUs from the order Bacteroidales, the genus Bacillariophyta and the genus Clostridium were found significantly more abundant in GZSD_H (14.9-22.8%) than in SVCP_H (0.13-4.1%) samples. These differences were presumably caused by the differences in the type of food sources including bacteria ingested, the gut morphology and digestion, and the physiological behavior between GZSD and SVCP.

Aspects of embryonic and larval development in bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix.

As bighead carp Hypophthalmichthysnobilis and silver carp H. molitrix (the bigheaded carps) are poised to enter the Laurentian Great Lakes and potentially damage the region's economically important fishery, information on developmental rates and behaviors of carps is critical to assessing their ability to establish sustainable populations within the Great Lakes basin. In laboratory experiments, the embryonic and larval developmental rates, size, and behaviors of bigheaded carp were tracked at two temperature treatments, one "cold" and one "warm". Developmental rates were computed using previously described stages of development and the cumulative thermal unit method. Both species have similar thermal requirements, with a minimum developmental temperature for embryonic stages of 12.1° C for silver carp and 12.9° C for bighead carp, and 13.3° C for silver carp larval stages and 13.4° C for bighead carp larval stages. Egg size differed among species and temperature treatments, as egg size was larger in bighead carp, and "warm" temperature treatments. The larvae started robust upwards vertical swimming immediately after hatching, interspersed with intervals of sinking. Vertical swimming tubes were used to measure water column distribution, and ascent and descent rates of vertically swimming fish. Water column distribution and ascent and descent rates changed with ontogeny. Water column distribution also showed some diel periodicity. Developmental rates, size, and behaviors contribute to the drift distance needed to fulfill the early life history requirements of bigheaded carps and can be used in conjunction with transport information to assess invasibility of a river.

Microsatellite genetic diversity and differentiation of native and introduced grass carp populations in three continents.

Grass carp (Ctenopharyngodon idella), a freshwater species native to China, has been introduced to about 100 countries/regions and poses both biological and environmental challenges to the receiving ecosystems. In this study, we analyzed genetic variation in grass carp from three introduced river systems (Mississippi River Basin in US, Danube River in Hungary, and Tone River in Japan) as well as its native ranges (Yangtze, Pearl, and Amur Rivers) in China using 21 novel microsatellite loci. The allelic richness, observed heterozygosity, and within-population gene diversity were found to be lower in the introduced populations than in the native populations, presumably due to the small founder population size of the former. Significant genetic differentiation was found between all pairwise populations from different rivers. Both principal component analysis and Bayesian clustering analysis revealed obvious genetic distinction between the native and introduced populations. Interestingly, genetic bottlenecks were detected in the Hungarian and Japanese grass carp populations, but not in the North American population, suggesting that the Mississippi River Basin grass carp has experienced rapid population expansion with potential genetic diversification during the half-century since its introduction. Consequently, the combined forces of the founder effect, introduction history, and rapid population expansion help explaining the observed patterns of genetic diversity within and among both native and introduced populations of the grass carp.