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.

     

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

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Multistate models of bigheaded carps in the Illinois River reveal spatial dynamics of invasive species

Knowledge of the spatial distributions and dispersal characteristics of invasive species is necessary for managing the spread of highly mobile species, such as invasive bigheaded carps (Bighead Carp [Hypophthalmichthys nobilis] and Silver Carp [H. molitrix]). Management of invasive bigheaded carps in the Illinois River has focused on using human-made barriers and harvest to limit dispersal towards the Laurentian Great Lakes. Acoustic telemetry data were used to parameterize multistate models to examine the spatial dynamics of bigheaded carps in the Illinois River to (1) evaluate the effects of existing dams on movement, (2) identify how individuals distribute among pools, and (3) gauge the effects of reductions in movement towards the invasion front. Multistate models estimated that movement was generally less likely among upper river pools (Starved Rock, Marseilles, and Dresden Island) than the lower river (La Grange and Peoria) which matched the pattern of gated versus wicket style dams. Simulations using estimated movement probabilities indicated that Bighead Carp accumulate in La Grange Pool while Silver Carp accumulate in Alton Pool. Fewer Bighead Carp reached the upper river compared to Silver Carp during simulations. Reducing upstream movement probabilities (e.g., reduced propagule pressure) by?≥?75% into any of the upper river pools could reduce upper river abundance with similar results regardless of location. Given bigheaded carp reproduction in the upper Illinois River is presently limited, reduced movement towards the invasion front coupled with removal of individuals reaching these areas could limit potential future dispersal towards the Great Lakes.     

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.     

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.     

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.     

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.     

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.

     

Predation and avoidance behaviour in aphid‐ladybird interactions of native and invasive ladybirds in Europe

1. While detrimental effects of invasive predators on native species are well documented, we often lack a mechanistic understanding of the invasion success. Lack of prey avoidance behaviour can lead to higher consumption rates by invasive predators compared to native predators. This competitive advantage is expected to contribute to the invasion success of non‐native predators.
2. We compared aphid consumption and cue avoidance behaviour of aphids between four native ladybird species (Coccinella septempunctata, Adalia bipunctata, Propylea quatuordecimpunctata, and Hippodamia variegata) and the invasive Asian ladybird Harmonia axyridis.
3. The invasive H. axyridis and the native C. septempunctata consumed more aphids than the three smaller native ladybird species. In line with our expectations, aphids avoided leaves bearing cues of most native ladybird species but not of the invasive H. axyridis.
4. Our results indicate that body size rather than ladybird origin determined aphid predation rates. The lack of aphid avoidance behaviour towards cues of H. axyridis indicates that they were not able to recognise the chemical cues of the invasive predator.
5. Relatively large body size and the absence of cue avoidance in aphids might benefit the invasive H. axyridis, particularly in comparison to smaller native ladybird species. The absence of avoidance behaviour in aphids might lead to even higher predation rates of H. axyridis under more natural conditions.

     

An invasive fish promotes invasive plants in Minnesota lakes

1. Biological invasions can greatly alter ecological communities, affecting not only the diversity and abundance but also composition of invaded assemblages. This is because invaders’ impacts are mediated by characteristics of resident species: some may be highly sensitive to invader impacts while others are unaffected or even facilitated. In some cases, this can result in invasive species promoting further invasions; in particular, herbivory by introduced animals has been shown to disproportionately harm native plants, which can indirectly benefit non-native plants. Here, we investigated whether such patterns emerged through the effects of an invasive fish species on lake plant communities.
2. Specifically, we tested whether invasion of Minnesota (U.S.A.) lakes by Cyprinus carpio (common carp), an omnivorous, benthivorous fish known to reduce abundance and richness of aquatic plants, differentially affected native versus non-native plant species. We applied statistical models to a large, long-term monitoring dataset (206 macrophyte taxa recorded in 913 lakes over a 20-year time period) to test whether carp altered community composition, to identify which macrophyte species were most sensitive to carp and determine whether species characteristics predicted carp sensitivity, and to characterise consequences of carp invasion on lake-level vegetation attributes.
3. We found that carp exerted strong selective pressure on community composition. Native macrophytes, those with a more aquatic growth form, and those considered less tolerant of disturbance (i.e. higher coefficients of conservatism) were more sensitive to carp. Conversely, no introduced macrophytes exhibited sensitivity to carp and all had higher probabilities of occurrence as carp abundance increased. The net effect of carp invasion was a shift toward less species-rich plant communities characterised by more non-native and disturbance-tolerant species.
4. These results have several implications for conservation and management. First, they reinforce the need to prevent further spread of carp outside of their native range. Where carp have already established, their control should be incorporated into efforts to restore aquatic vegetation; this may be an essential step for recovering particular plant species of high conservation importance. Furthermore, reducing carp abundance could have ancillary benefits of reducing dominance by invasive plant species. Lastly, where carp cannot be eliminated, managers should target native macrophytes that are relatively tolerant of carp in shoreline plantings and other revegetation efforts.

     

A molecular approach to detect hybridisation between crucian carp (Carassius carassius) and non-indigenous carp species (Carassius spp. and Cyprinus carpio)

1. Releases of non‐native fish into the wild is an increasing problem posing considerable ecological and genetic threats through direct competition and hybridisation. 2. We employed six microsatellite markers to identify first generation hybrids and backcrosses between native crucian carp (Carassius carassius) and introduced goldfish (C. auratus) and common carp (Cyprinus carpio) in the U.K. We also investigated the genetic characteristics of the taxonomically controversial gibel carp (Carassius spp.) from sites across Europe. 3. Natural hybridisation between goldfish and crucian carp occurs frequently, although hybrids between all other species pairs were observed. Only 62% of British crucian carp populations (n = 21) consisted exclusively of pure crucian carp. In some populations hybrids were so frequent, that no pure crucian carp were caught, indicating a high competitive ability of hybrids. 4. Most hybrids belonged to the F1 generation but backcrossing was evident at a low frequency in goldfish × crucian carp hybrids and goldfish × common carp hybrids. Furthermore, some local populations had high frequencies of backcrosses, raising the opportunity for introgression. 5. Gibel carp from Germany and Italy belonged to two triploid clonal lineages that were genetically closely related to goldfish, whereas all individuals identified from British populations proved to be crucian carp × goldfish hybrids. 6. Our study suggests that the release of closely related exotic cyprinids not only poses a threat to the genetic integrity and associated local adaptations of native species, but may also contribute to shifts in community structure through competitive interactions.     

Filamentous cyanobacteria alter the relative fitness in a Daphnia hybrid species complex

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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.     

Lake Michigan's suitability for bigheaded carp: The importance of diet flexibility and subsurface habitat

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Decline of unionid mussels enhances hybridisation of native and introduced bitterling fish species through competition for breeding substrate

1. Bitterling fishes (Subfamily: Acheilognathinae) spawn in the gills of living freshwater mussels and obligately depend on the mussels for reproduction. On the Matsuyama Plain, Japan, populations of unionid mussels—Pronodularia japanensis, Nodularia douglasiae, and Sinanodonta lauta—have decreased rapidly over the past 30 years. Simultaneously, the population of a native bitterling fish, Tanakia lanceolata, which depends on the three unionids as a breeding substrate, has decreased. Furthermore, a congeneric bitterling, Tanakia limbata, has been artificially introduced, and hybridisation and genetic introgression occur between them. Here, we hypothesised that decline of the unionids has enhanced this invasive hybridisation through competition for the breeding substrate.
2. Three study sites were set in three streams on the Matsuyama Plain. We collected adult bitterling fishes (native T. lanceolata, introduced T. limbata, and foreign Rhodeus ocellatus ocellatus) once a week from April to October 2013 to measure their densities in streams and to examine seasonal differences in female ovipositor length, which elongates in the breeding season. Simultaneously, we set quadrats and captured unionids and measured environmental conditions. Each unionid individual was kept separately in its own aquarium to collect ejected bitterling eggs/larvae. Tanakia eggs and larvae were genotyped using six microsatellite markers and the mitochondrial cytochrome b gene.
3. Introduced T. limbata was more abundant, had a longer breeding period, and produced more juveniles than native T. lanceolata. Hybrids between the two species occurred at all sites, and in total 101 of the 837 juveniles genotyped were hybrids. The density of P. japanensis was low, at most 0.42 individuals/m². Nodularia douglasiae and S. lauta have nearly or totally disappeared from these sites. Hybrid clutches of Tanakia species occurred more frequently where the local density of P. japanensis was low. Mussels were apparently overused and used simultaneously by three species of bitterlings.
4. Decline of freshwater unionid populations has enhanced hybridisation of native and invasive bitterling fishes through increasing competition for breeding substrate. We showed that rapid decline of host mussel species and introduction of an invasive congener have interacted to cause a rapid decline of native bitterling fish.
5. Degradation of habitat and the introduction of invasive species interact to cause a cascade of extinctions in native species. In our study, obligate parasite species are threatened because the host species are disappearing, which means there is a serious threat of coextinction.

     

Breakdown of species boundaries in Mandevilla: floral morphological intermediacy,novel fragrances and asymmetric pollen flow

• Phenotypic intermediacy is an indicator of putative hybrid origin and has provided the main clues to discovering hybrid plants in nature. Mandevilla pentlandiana and M. laxa (Apocynaceae) are sister species with clear differences in floral phenotype and associated pollinator guilds: diurnal Hymenoptera and nocturnal hawkmoths, respectively. The presence of individuals with intermediate phenotypes in a wild population raises questions about the roles of visual and olfactory signals (i.e. corolla morphology and floral fragrances) as barriers to interbreeding, and how the breakdown of floral isolation occurs.
• We examined phenotypic variation in a mixed Mandevilla population, analysing the chemical composition of floral fragrances, characterising floral shape through geometric morphometrics and assessing individual grouping through taxonomically relevant traits and an unsupervised learning algorithm. We quantified the visitation frequencies of floral visitors and tracked their foraging movements using pollen analogues.
• The presence of morphologically intermediate individuals and pollen analogue movement suggested extensive hybridisation between M. laxa and M. pentlandiana, along with asymmetrical rates of backcrossing between these putative hybrids and M. laxa. Floral volatiles from putative hybrid individuals showed a transgressive phenotype, with additional compounds not emitted by either parental species.
• Our results suggest the presence of a hybrid swarm between sympatric M. pentlandiana and M. laxa and indicate that initial hybridisation events between these parental species are rare, but once they occur, visits between putative hybrids and M. laxa are common and facilitate continued introgression.

     

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

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