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.     

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.     

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.     

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.     

Bigheaded carps (<Emphasis Type="Italic">Hypophthalmichthys</Emphasis> spp.) at the edge of their invaded range: using hydroacoustics to assess population parameters and the efficacy of harvest as a control strategy in a large North American river

The threat posed by bigheaded carps (Hypophthalmichthys spp.) to novel ecosystems has focused efforts on preventing further range expansion; upstream progression in the Illinois River is a major concern due to its connection with the uninvaded Great Lakes. In addition to an electric barrier system, commercial harvest of silver carp (H. molitrix) and bighead carp (H. nobilis) in the upper river is intended to reduce propagule pressure and prevent range expansion. To quantify demographics and evaluate harvest efficacy, the upper river was sampled between 2012 and 2015 using mobile hydroacoustic methods. Reach-specific densities, size structures and species compositions varied interannually but the advancing population was characterized longitudinally as small-bodied, silver carp-dominated at the highest densities downstream, shifting to large-bodied, bighead carp-dominated at the low-density population front. The use of hydroacoustic sampling for harvest evaluation was validated in backwater lakes; there was a significant positive correlation between density estimates and the corresponding harvest catch-per-unit-effort of bigheaded carps. Localized densities of bigheaded carps were reduced by up to 64.4 % immediately post-harvest but generally rebounded within weeks. However, annual sampling of the entire upper river indicated that density of bigheaded carps decreased by over 40 % (between 2012 and 2013) and subsequently remained stable (between 2013 and 2014). The annual harvest of bigheaded carps increased during this period (from 45,192 to 102,453 individuals), in years of contrasting discharge conditions. At this spatiotemporal scale, harvest appears to have contributed to initial reduction, and subsequent maintenance of, bigheaded carps density levels, but discharge likely plays an important role (e.g., through immigration) in determining the extent of its impact. Mobile hydroacoustic sampling enabled robust quantification of the population over varying spatial scales and density gradients, highlighting the potential of this approach as an assessment tool for invasive fishes in riverine environments.     

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.

     

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.

     

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.     

The facilitation of the native bluegill sunfish by the invasive bighead carp

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Temperature dependent effects of carbon dioxide on avoidance behaviors in bigheaded carps

Effective behavioral deterrents are needed to prevent aquatic invasive species from entering novel ecosystems. One deterrent strategy that shows promise is elevated carbon dioxide (CO₂) concentrations in water which can alter the behavior of freshwater fishes, including invasive bigheaded carps (Hypophthalmichthys spp.). However, few studies have evaluated behavioral responses to elevated CO₂ concentrations at different water temperatures. The objective of this study was to quantify CO₂ concentrations needed to achieve avoidance (voluntary response) and narcosis (involuntary response observed by loss of equilibrium) behaviors in silver carp (H. molitrix) and bighead carp (H. nobilis) at 5, 15, and 25 °C. Overall, silver carp and bighead carp displayed avoidance and narcosis behaviors to CO₂ at each water temperature, however bighead carp responded at higher CO₂ concentrations than silver carp. Behavioral avoidance and narcosis were observed at approximately 40% lower CO₂ concentrations in 5 °C water relative to 25 °C suggesting considerable influence of water temperature on a CO₂ stimulus for both species. Results indicate that fluctuating water temperature (e.g., spatial and temporal variation across management sites) can influence how fish respond to elevated CO₂, and may usefully be considered when applying CO₂ as a behavioral deterrent.     

Native bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix populations in the Pearl River are threatened by Yangtze River introductions as revealed by mitochondrial DNA

Bighead carp Hypophthalmichthys nobilis and silver carp Hypophthalmichthys molitrix have been two economically important aquaculture species in China for centuries. In the past decades, bighead and silver carp have been introduced from the Yangtze River to many river systems in China, including the Pearl River, in annual, large-scale, stocking activities to enhance wild fisheries. Nonetheless, few studies have assessed the ecological or genetic impacts of such introductions on native conspecific fish populations. An mtDNA D-loop segment of 978 bp from 213 bighead carp samples from 9 populations and a 975 bp segment from 204 silver carp samples from 10 populations were obtained to evaluate genetic diversity and population integrity. Results from a haplotype network analysis revealed that most haplotypes of the Pearl River clustered with those of Yangtze River origin and only a small proportion were distinct, suggesting that both the native Pearl River bighead and silver carp populations are currently dominated by genetic material from the Yangtze River. The genetic diversity of Pearl River populations is high in both species because of this inter-population gene flow, but the diversity of native Pearl River populations is low. To preserve the native genetic diversity, stocking of non-native fingerlings should cease immediately and native Pearl River bighead and silver carp fish farms should be established. This research demonstrates the danger to native biodiversity across China because of the substantial, ongoing stock-enhancement activities without prior genetic assessment.     

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.

     

Size‐specific effects of bighead carp predation across the zooplankton size spectra

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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.     

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.     

Can filter‐feeding Asian carp invade the Laurentian Great Lakes? A bioenergetic modelling exercise

1. There is much concern that filter‐feeding Asian carp will invade the Laurentian Great Lakes and deplete crucial plankton resources. We developed bioenergetic models, using parameters from Asian carp and other fish species, to explore the possibility that planktonic food resources are insufficient to support the growth of silver carp (Hypophthalmichthys molitrix) and bighead carp (H. nobilis) in the Great Lakes. 2. The models estimated basic metabolic requirements of silver and bighead carp under various body sizes, swimming speeds and reproductive stages. These requirements were then related to planktonic food resources and environmental temperature to predict when and where silver and bighead carp may survive in the Great Lakes, and how far they may travel. 3. Parameter values for respiration functions were derived experimentally in a coordinated study of silver and bighead carp, while consumption parameters were obtained from the literature on silver carp. Other model parameters lacking for Asian carp, such as those for egestion and excretion, were obtained from the literature on other fish species. 4. We found that full‐sized bighead carp required 61.0 kJ d^?1 just to maintain their body mass at 20 °C, approximately equivalent to feeding in a region with 255 μg L^?1 macrozooplankton (dry) or 10.43 μg L^?1 chlorophyll a. Silver carp energy requirements were slightly higher. 5. When applied to various habitats in the Great Lakes, our results suggest that silver and bighead carp will be unable to colonise most open‐water regions because of limited plankton availability. However, in some circumstances, carp metabolism at lower temperatures may be low enough to permit positive growth even at very low rations. Positive growth is even more likely in productive embayments and wetlands, and the modelled swimming costs in some of these habitats suggest that carp could travel >1 km d^?1 without losing biomass. 6. The simulation (and firmly hypothetical) results from this modelling study suggest when and where Asian carp could become established in the Great Lakes. Given the potential consequences to Great Lakes ecosystems if these filter feeders do prove capable of establishing reproducing populations, efforts to keep Asian carp out of the Great Lakes must not be lessened. However, we do encourage the use of bioenergetic modelling in a holistic approach to assessing the risk of Asian carp invasion in the Great Lakes region.     

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.

     

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.