Diagnostic SNPs reveal widespread introgressive hybridization between introduced bighead and silver carp in the Mississippi River Basin

Hybridization among conspecifics in native and introduced habitats has important implications for biological invasions in new ecosystems. Bighead (Hypophthalmichthys nobilis) and silver carp (H. molitrix) are genetically isolated and occur in sympatry within their native range. Following their introduction to North America, however, introgressant hybrids have been reported throughout their expanded range within the Mississippi River Basin (MRB). The extent of introgression, both spatially and generationally, is largely unknown. Therefore, we examined mixed‐species populations from across the MRB to characterize the extent of interspecific gene flow. We assayed 2798 individuals from nine locations with a suite of species‐diagnostic SNPs (57 nuclear and one mitochondrial). Forty‐four per cent (n = 1244) of individuals displayed hybrid genotypes. Moreover, the composition of hybrid genotypes varied among locations and represented complex hybrid swarms with multiple generations of gene flow. Introgressive hybrids were identified from all locations, were bidirectional and followed a bimodal distribution consisting primarily of parental or parental‐like genotypes and phenotypes. All described hybrid categories were present among individuals from 1999 to 2008, with parents and later‐generation backcrosses representing the largest proportion of individuals among years. Our mitochondrial SNP (COII), tested on a subset of 730 individuals, revealed a silver carp maternal bias in 13 of 21 (62%) F₁ hybrids, in all silver carp backcrosses, and maintained throughout many of the bighead carp backcrosses. The application of this suite of diagnostic markers and the spatial coverage permits a deeper examination of the complexity in hybrid swarms between two invasive, introduced species.     

Tag retention and survival of juvenile bighead carp implanted with a dummy acoustic tag at three temperatures

Bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix (together, the bigheaded carps) are invasive fishes in North America that have resulted in substantial negative effects on native fish communities and aquatic ecosystems. Movement and behavior of adult bigheaded carps has been studied previously using telemetry, while similar studies with juvenile bigheaded carps have yet to be attempted. Recent technological advances in telemetry transmitters has increased the availability of tags sufficiently small enough to implant in juvenile carps. However, the effects of surgical implantation of telemetry tags on juvenile bigheaded carps have not been evaluated. We determined tag retention and survival associated with surgical implantation of acoustic telemetry tags into juvenile bighead carp (range 128–152 mm total length) at three temperatures (13, 18, and 23°C). In addition, we assessed the effect of surgically implanted transmitters on the fitness, defined as changes in weight or critical swimming speed, of carp implanted with transmitters. Survival was high among tagged fish (85%) with 47% of tags retained at the conclusion of the 45‐day study. No substantial decline in fitness of the fish was observed in tagged fish compared to untagged fish.     

Body condition (Wr) and reproductive potential of bighead and silver carp hybrids: Postzygotic selection in the Mississippi River Basin

Invasive bighead (Hypophthalmichthys nobilis) and silver carp (H. molitrix) are reproductively isolated in their native range, but form a bimodal, multigenerational hybrid swarm within the Mississippi River Basin (MRB). Despite observed F₁ hybrid superiority in experimental settings, effects of postzygotic selection on bighead and silver carp hybrids have not been tested in a natural system. Individual parent and hybrid genotypes were resolved at 57 species‐specific loci and used to evaluate postzygotic selection for body condition (W_r) and female reproductive potential (presence of spawning stage gonads and gonadosomatic index [GSI]) in the MRB during 2009–2011. Body condition in the Marseilles Reach, Illinois River declined with a decrease in species‐specific allele frequency from 1.0 to 0.4 for each species and early generation hybrids (F₁, F₂, and first‐generation backcross) had lower mean W_r than late generation hybrids (2nd+ generation backcrosses) and parentals. Proportions of stage IV and stage V (spawning stage) female gonads differed between bighead and silver carp, but not among parentals and their early and late generation hybrids within the MRB. Mean GSI values did not differ between parentals and hybrids. Because reproductive potential did not differ between hybrids and parentals, our results suggest that early generation hybrids occur in low frequency either as a factor of poor condition (W_r) and postreproductive survival, infrequent reproductive encounters by parental bighead and silver carp, or selection pressures acting on juvenile or immature life stages. Our results suggest that a combination of genetic and environmental factors may contribute to the postzygotic success of bighead and silver carp hybrids in the Mississippi River Basin.     

Persistence of DNA in Carcasses,Slime and Avian Feces May Affect Interpretation of Environmental DNA Data

The prevention of non-indigenous aquatic invasive species spreading into new areas is a goal of many resource managers. New techniques have been developed to survey for species that are difficult to capture with conventional gears that involve the detection of their DNA in water samples (eDNA). This technique is currently used to track the invasion of bigheaded carps (silver carp and bighead carp; Hypophthalmichthys molitrix and H. nobilis) in the Chicago Area Waterway System and Upper Mississippi River. In both systems DNA has been detected from silver carp without the capture of a live fish, which has led to some uncertainty about the source of the DNA. The potential contribution to eDNA by vectors and fomites has not been explored. Because barges move from areas with a high abundance of bigheaded carps to areas monitored for the potential presence of silver carp, we used juvenile silver carp to simulate the barge transport of dead bigheaded carp carcasses, slime residue, and predator feces to determine the potential of these sources to supply DNA to uninhabited waters where it could be detected and misinterpreted as indicative of the presence of live bigheaded carp. Our results indicate that all three vectors are feasible sources of detectable eDNA for at least one month after their deposition. This suggests that current monitoring programs must consider alternative vectors of DNA in the environment and consider alternative strategies to minimize the detection of DNA not directly released from live bigheaded carps.     

Early generation hybrids may drive range expansion of two invasive fishes

1. Introgressive hybridisation between two invasive species has the potential to contribute to their invasion success and provide genetic resiliency to rapidly adapt to new environments. Additionally, differences in the behaviour of hybrids may lead to deleterious ecosystem effects that compound any negative impacts of the invading parental species.
2. Invasive silver carp (Hypophthalmichthys molitrix) and bighead carp (Hypophthalmichthys nobilis) provide an opportunity to evaluate how hybridisation may influence the behaviour, dispersal, and spread of an invasive species introgressive complex. In order to investigate the role hybrids may have in the invasion ecology of bigheaded carps, we examined the distribution, movements, and environmental cues for movement of two invasive fishes and their hybrids in the Illinois River (U.S.A.).
3. Early generation hybrids (e.g. F₁,F₂, and first-generation backcross individuals) composed a greater proportion of the population at the invasion front where abundances of bigheaded carp were low. A greater proportion of early hybrids passed through dams upstream towards the invasion front than did other hybrids and parental species.
4. The movements and environmental cues for movement of late-generation backcrosses (more genetically similar to parental genotype) were not different from the parental species with which they shared the most alleles. Although the direction of the relationship between movement and environment was sometimes different for the parental species and associated advanced generation hybrids, these results indicate that management for parental species will also affect most hybrids.
5. Although early generation hybrids are rare, our results indicate they may disperse towards low-density population zones (i.e. invasion fronts) or are produced at greater frequency in low-density areas. These rare hybrids have the potential to produce a variety of unique genetic combinations that could result in more rapid adaptation of a non-native population to their invaded range potentially facilitating the establishment of invasive species.

     

Trophic reorganization of native planktivorous fishes at different density extremes of bigheaded carps in the Illinois and Mississippi rivers,USA

The widespread introduction of non-native fishes has contributed to freshwater ecosystems being considered among the most altered ecosystems globally. Of particular concern are invasive planktivorous fishes (e.g., silver carp Hypophthalmichthys molitrix and bighead carp H. nobilis, collectively known as bigheaded carps) that have the potential to modify basal food web structure and compete for planktonic resources with native planktivores and young-of-year fishes. Bigheaded carps have proliferated throughout the Mississippi River basin, creating an outsized potential for resource competition with native fishes. Studies have showed niche overlap between bigheaded carps and native planktivores is generally high but that overlap varies among rivers. Importantly, niche overlap has not been assessed for density extremes of bigheaded carps within a river to determine whether trophic niches changed as a result of the invasion. The objectives of this study were to determine whether (1) silver and/or bighead carps share a similar isotopic niche with four native planktivores, and (2) that association varies ecologically (i.e., low- and high-densities of bigheaded carps) and spatially (i.e., between rivers). Our results generally show high trophic overlap among species, suggesting potential direct resource competition. Niche overlap was higher in study reaches with low densities of bigheaded carps compared to reaches with high densities, presumably due to intense resource competition and limiting of resources under high densities of bigheaded carps. Across density extremes, trophic reorganization by bigmouth buffalo (Ictiobus cyprinellus) was divergent from other native planktivores. Species-specific responses may be due to subtle differences in feeding strategies, degree of planktivory, food selectivity, and correlated food size distributions.

     

Swimming performance of adult bighead carp Hypophthalmichthys nobilis (Richardson, 1845) and silver carp H. molitrix (Valenciennes, 1844)

Although the movement of invasive bighead carp (Hypophthalmichthys nobilis) and silver carp (H. molitrix) in the Upper Mississippi River system is dependent on their ability to swim through its numerous lock‐and‐dams, the swimming performance of adults of these species is at present unknown. Using a large (2,935‐L) mobile swim tunnel, the swimming performance of adult bighead and adult silver carp was quantified at water velocities that challenged them to exhibit either prolonged and/or burst swimming (76–244 cm/s) with fatigue times of less than 10 min. Simple log‐linear models best described the relative swim speed to fatigue relationships for both species. Under these conditions, the swimming performances of adult bighead and silver carp were similar to several species of adult fishes native to the Mississippi River system, but relatively low (<3 total body lengths per second, TL/s) compared to previously studied juveniles and sub‐adult bigheaded carps (3–15 TL/s). The decline in endurance with water velocity was three times greater in bighead carp (slope = ?2.98) than in silver carp (slope = ?1.01) and the predictive ability of the bighead model was appreciably better than the silver carp model. The differences in adult swimming performance between the two species were coincident with behavioral differences (e.g. breaching in silver carp but not in bighead carp). The swimming performance data of adult bighead and silver carp can now be used to evaluate whether their passage through manmade river structures including the gates of lock‐and‐dams in the Upper Mississippi River might be reduced.     

Phenotypic plasticity in the spawning traits of bigheaded carp (Hypophthalmichthys spp.) in novel ecosystems

1. Bigheaded carp, including both silver (Hypophthalmichthys molitrix) and bighead (H. nobilis) carp, are successful invasive fishes that threaten global freshwater biodiversity. High phenotypic plasticity probably contributes to their success in novel ecosystems, although evidence of plasticity in several spawning traits has hitherto been largely anecdotal or speculative. 2. We collected drifting eggs from a Midwestern U.S.A. river from June to September 2011 and from April to June 2012 to investigate the spawning traits of bigheaded carp in novel ecosystems. 3. Unlike reports from the native range, the presence of drifting bigheaded carp eggs was not related to changes in hydrological regime or mean daily water temperature. Bigheaded carp also exhibited protracted spawning, since we found drifting eggs throughout the summer and as late as 1 September 2011. Finally, we detected bigheaded carp eggs in a river reach where the channel is c. 30 m wide with a catchment area of 4579 km², the smallest stream in which spawning has yet been documented. 4. Taken with previous observations of spawning traits that depart from those observed within the native ranges of both bighead and silver carp, our findings provide direct evidence that bigheaded carp exhibit plastic spawning traits in novel ecosystems that may facilitate invasion and establishment in a wider range of river conditions than previously envisaged.     

Modelling bioenergetic and population-level impacts of invasive bigheaded carps (Hypophthalmichthys spp.) on native paddlefish (Polyodon spathula) in backwaters of the lower Mississippi River

1. While invasions of large rivers by exotic fish species are well documented, assessing actual or potential impacts on native species is a challenge. Rapid assessments may be possible through the application of a combination of bioenergetic and population dynamic models.
2. Paddlefish (Polyodon spathula) is a native species in the central USA with a history of population decline due to waterway development and overharvesting for roe. It is not known whether paddlefish are impacted by resource competition from invasive bigheaded carp populations, including silver (Hypophthalmichthys molitrix) and bighead carp (Hypophthalmichthys nobilis), which have expanded dramatically in the Mississippi River.
3. We used bioenergetic models to project the potential impact of invasive silver and bighead carp on zooplankton density and paddlefish somatic growth in backwater habitat. Bioenergetic outputs were translated to impacts on fecundity, becoming inputs for 50-year metapopulation simulations of backwater habitat connected to the main-stem Mississippi River by episodic flood events.
4. Competition with carp reduced growth and increased the risk of population decline for paddlefish. Impacts increased disproportionately with increased carp abundance and were further exacerbated in scenarios with increased diet overlap or decreased zooplankton abundance.
5. We also analysed paddlefish condition data collected at sites near the lower Mississippi River with varying histories of carp invasion. These data give credence to the bioenergetic model output; paddlefish had reduced body condition at sites with long-established, high-density carp populations.
6. We conclude that invasive bigheaded carps have great potential to reduce paddlefish growth, fecundity, and abundance. The pairing of bioenergetics and population models is likely to be broadly useful in assessing the risks posed by other invasive species.

     

Ingestion of bacteria in suspension Indian major carps (Catla catla,Labeo rohita) and Chinese carps (Hypophthalmichthys molitrix,Aristichthys nobilis)

Single-species groups of fry of the planktivorous, filter-feeding carps (silver carp Hypophthalmichthys molitrix, bighead carp Aristichthys nobilis, rohu Labeo rohita and catla Catla catla) were exposed to the bacterium Chromobacterium violaceum to assess if they could detect or ingest unattached bacteria. The results indicate that planktivorous carp fry are able to ingest unattached bacteria and that the numbers ingested increase with time and with bacterial concentration in the media, although probably by passive means. It is also suggested that unattached bacteria are of little nutritional significance to carps.     

Aspects of Embryonic and Larval Development in Bighead Carp Hypophthalmichthys nobilis and Silver Carp Hypophthalmichthys molitrix

As bighead carp Hypophthalmichthys nobilis 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.     

Anticipating the spread and ecological effects of invasive bigheaded carps (<Emphasis Type="Italic">Hypophthalmichthys</Emphasis> spp.) in North America: a review of modeling and other predictive studies

Bighead carp (Hypophthalmichthys nobilis Valenciennes 1844) and silver carp (H. molitrix Richardson 1845), collectively called bigheaded carps, have invaded the Mississippi River Basin and may have already entered the Laurentian Great Lakes where they could affect fishing and other industries. Developing models to predict potential spread and effects is difficult because local adaptation may have occurred among populations, parameter values for biological characteristics vary widely for these opportunistic generalists, and methodological differences complicate comparison and synthesis of studies. I review bigheaded carp biological parameters across a wide range of literature, including studies of native and introduced populations. I then evaluate how predictive models are parameterized, noting inconsistencies and highlighting data gaps. My analysis finds that although parameter values tend to vary substantially among and within systems, models are generally parameterized using the best information available, although bioenergetics and trophic models particularly need improvement. Some predictive tools can be updated using existing data (e.g., velocity requirements for spawning), but in other cases further research is needed. Research priorities include (1) better understanding bigheaded carp phenotypic plasticity among and within systems, (2) determining key biological traits of bigheaded carp populations at risk of seeding further invasions (e.g., Illinois River populations that may spread to Lake Michigan), and (3) monitoring bigheaded carp ecological effects on native fishes and plankton communities. A more complete awareness of strengths and limitations of predictive tools will lead to their improvement, thereby aiding managers in anticipating and counteracting bigheaded carp spread and effects.     

Reproductive condition and occurrence of intersex in bighead carp and silver carp in the Missouri River

Little is known about the reproductive biology of the exotic bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix in the Missouri River. In order to fill this gap in understanding, herein is described the reproductive condition of these Asian carps. Evidence is presented which indicates that bighead and silver carp in the Missouri River have a protracted spawning period that extends from early spring through fall and some individual bighead and silver carp are spawning multiple times during a reproductive season. Although bighead and silver carps are successfully maturing and spawning in the Missouri River some reproductive abnormalities such as intersex, atresia, and sterility were observed. Knowledge of the reproductive activity of these invasive carps may be useful to resource managers tasked with their control. Furthermore, the reproductive abnormalities observed should be considered when evaluating the environmental condition of the Missouri River relative to supporting a healthy fish fauna.     

Comparative studies on carcass characteristics of marketable size farmed mrigal Cirrhinus mrigala, (Hamilton, 1822), and silver carp Hypophthalmichthys molitrix, (Val., 1844)

The carcass traits and commercial characteristics of farmed freshwater Cirrhinus mrigala and Hypophthalmichthys molitrix were investigated to calculate yield data useful for programming semi‐automated processing units. Specimens with average weights of 2500 and 3400 g were collected from both mrigal and silver carps, respectively. Samples were taken from grow‐out culture ponds of the Central Institute of Freshwater Aquaculture (CIFA), Odisha State, India. Carcass and offal yields as well as carcass cutability were assessed. Head yields were recorded as 14.9 and 27.5% for mrigal and silver carp, respectively. The gutted yield, headless yield and skinless dressed round percentages were determined as 89.4, 74.5 and 67.6% for mrigal and 92.8, 65.4 and 62.0% for silver carps, respectively. The meat: bone ratio in filleting averaged 4.8 for mrigal and 3.1 for silver carp. The middle cut of mrigal had both the highest total yield percentage and highest meat yield, whereas this was equally distributed between both the fore and middle cuts in silver carp. In both mrigal and silver carp the dry matter, ether extract and protein percentages were highest in the fore cut followed by middle and hind cut. In silver carp the percentage fat content was found to be significantly higher than in mrigal.     

Using marketing to fish‐down bigheaded carp (Hypophthalmichthys spp.) in the United States: Eliminating the negative brand name, “carp”

Invasive bigheaded carp species (Hypophthalmichthys spp.) from Asia have experienced rapid range expansion and population explosions in rivers of the United States resulting in ecosystem damage currently being witnessed and documented by fishery biologists. In addition, silver carp (H. molitrix) present a danger of injury and death to unsuspecting boaters, water skiers or recreational fishers due to their propensity to jump in response to boat motor noise. Fishing‐down bigheaded carp populations for human consumption will reduce environmental damage and potential human injury and mortality until other control measures become available. The name “carp” conveys an extremely negative brand name for purposes of product marketing. We suggest that the silver carp be renamed by the professional scientific community to silverfin (a trademarked name currently used in culinary circles) and the bighead carp (H. nobilis) to bighead. The suggested common names changes represent a simple, albeit small step to reducing bigheaded carp population numbers based on sound product naming strategies developed and used in marketing science.     

Influence of environmental factors and individual traits on the diet of non-native hybrid bigheaded carp (Hypophthalmichthys molitrix × H. nobilis) in Lake Balaton,Hungary

Planktivorous silver carp and bighead carp (collectively, the bigheaded carps) have been stocked worldwide and their invasion has caused severe impacts on many freshwater ecosystems. Exploiting the chance provided by the specific hybrid bigheaded carp stock in Lake Balaton (Hungary) covering the entire morphological range between the two species (including gill raker morphology), we implemented a comprehensive study (1) to reveal the feeding habits of hybrid bigheaded carps living in a mesotrophic, lacustrine habitat and (2) to assess how biotic and abiotic environmental factors and gill raker morphology affect diet composition. We found that all bigheaded carps utilized primarily zooplankton and neglected the scarce and inefficiently digestible phytoplankton, irrespective of gill raker morphology. Moreover, we observed strikingly high levels of inorganic debris consumption, but the proportion of inorganic matter in the guts was not associated directly with the concentration of suspended inorganic particles. Variance in the diet composition of bigheaded carps was related mostly to environmental factors, including the wind-induced resuspension of inorganic particles and seasonally variable availability of food resources. In conclusion, the effects of abiotic environmental factors and available food resources could overwhelm the effect of gill raker morphology in shaping the feeding habits of bigheaded carps.

     

Introduction and cage culture of exotic carps and their impact on fish harvested in Lake Begnas,Nepal

The suitability of exotic carps namely Aristichthys nobilis (Bighead carp), Hypophthalmichthys molitrix (Silver carp), Ctenopharyngodon idellus (Grass carp), Cyprinus carpio (Common carp) and Labeo rohita (Rohu) in a sub-tropical lake was evaluated. The impact of their introduction on native fishes was also studied. After the introduction and cage culture of exotic carps the total harvest reached 92 kg·ha^–1; an increase of 266% within eight years. The planktivorous bighead and silver carps were most successful. The harvest of the other three species was poor. Since the introduction of exotic carp the harvest of indigenous fishes declined by 42%. Considering the food habits of these fish, further stocking should be limited to bighead and silver carps to limit the adverse effects on the indigenous species.