Performance as a fish predator of largemouth bass [<Emphasis Type="Italic">Micropterus salmoides</Emphasis> (Lacepède)] invading Japanese freshwaters: a review

This review focuses on how predator performance of the invasive largemouth bass [Micropterus salmoides (Lacepède)] has been, or will be, formed in Japanese freshwaters. Predation impacts of largemouth bass on fish communities appear pervasive in both Japanese as well as North American freshwaters. Factors affecting performance as a piscivorous predator are (1) light intensity and water clarity, (2) oxygen depletion, (3) prey size and gape size, (4) behavioral refuge of prey, (5) weed beds as refuge for prey fish, (6) interaction with bluegill. Size and behavioral refuges requirements are so rigorous that they may have evolved only in some North American prey fish species like bluegill; therefore, most Japanese native fish species are unlikely to be equipped with such refuges. However, refuge habitats like aquatic weed beds could develop in Japanese freshwaters, allowing prey fish species to survive under predation pressure. The density, architecture, and species composition of aquatic plants may affect their suitability as refuges. Studies in Japanese waters have suggested that the presence of rich aquatic vegetation or invasive bluegill in bass-introduced waters have suppressed the predation impact of largemouth bass on fish communities. In addition to these environmental factors, original genotypic and phenotypic traits of the introduced largemouth bass, and hybridization between different lineages of largemouth bass or with Florida bass [Micropterus floridanus (Lesueur)] may be involved in further adaptation of invasive largemouth bass to Japanese freshwaters.     

Predation of Japanese dace, Tribolodon hakonensis, by largemouth bass, Micropterus salmoides, in experimental aquaria

 To test the size range of prey fish that largemouth bass, Micropterus salmoides, can successfully consume, live Japanese dace, Tribolodon hakonensis, were given as prey fish to individual largemouth bass in aquaria. The ratio of maximum standard length (SL) of the Japanese dace consumed by largemouth bass was 46–69% of bass SL. The maximum length of Japanese dace consumed did not differ significantly between largemouth bass and smallmouth bass (M. dolomieu) previously studied, although largemouth bass have relatively larger mouth sizes than smallmouth bass. Largemouth bass occasionally injured and killed Japanese dace larger than the limit that could be consumed.     

Effects of turbidity and an invasive waterweed on predation by introduced largemouth bass

Anthropogenic activities lead to changes in characteristics of aquatic ecosystems, including alteration of turbidity and addition of invasive species. In this study, we tested how changes in turbidity and the recent invasion of an aquatic macrophyte, Egeria densa, may have changed the predation pressure by introduced largemouth bass on juvenile striped bass and delta smelt, two species that have seen a drastic decline in recent decades in the Sacramento-San Joaquin Delta. In a series of mesocosm experiments, we showed that increases in vegetation density decreased the predation success of largemouth bass. When placed in an environment with both open water and vegetated areas, and given a choice to forage on prey associated with either of these habitats, largemouth bass preyed mainly on open water species as opposed to vegetation-associated species, such as juvenile largemouth bass, bluegill or red swamp crayfish. Finally, we showed that turbidity served as cover to open water species and increased the survival of delta smelt, an endemic species at risk. We also found that such open water prey tend not to seek refuge in the vegetation cover, even in the presence of an imminent predation threat. These results provide the beginning of a mechanistic framework to explain how decreases in turbidity and increases in vegetation cover correlate with a decline of open water species in the Sacramento-San Joaquin Delta.     

Aggregation Behavior in Wildtype and Transgenic Zebrafish

Recent advances in the development and availability of genetically modified animals enable researchers to examine the effects of phenotypic characters on social behavior. In fish, shoaling behavior is known to be influenced by characteristics such as body coloration, striping pattern, body shape, and size. GloFish^TM are genetically engineered zebrafish (Danio rerio) that express red fluorescent protein (RFP), resulting in on overall red coloration under the dark longitudinal stripes. The GloFish pattern is distinct from the light body coloration underlying the dark longitudinal stripes seen in wildtype zebrafish. We presented wildtype and transgenic RFP zebrafish with same‐sex shoals of both strains of fish in dichotomous choice tests. No preference for either of the shoals was shown, however, both strains showed significant preferences for swimming near shoals vs. swimming near an empty tank compartment. When presented with opposite‐sex individuals of both strains, no preference was shown by either sex of either strain. Thus, the red body coloration of transgenic zebrafish does not appear to affect choice of social partner, in either a shoaling or a potentially reproductive context.     

Projected US distributions of transgenic and wildtype zebra danios, Danio rerio, based on temperature tolerance data

A genetically modified version of the south Asian, zebra danio, Danio rerio, a common aquarium fish, has become the first transgenic pet sold in the USA. Mean chronic lethal maxima of wildtype (39.8 °C, n=16$n=16$) and transgenic (39.3 °C, n=10$n=10$) zebra danios initially acclimated to 30 °C were statistically (but not dramatically) different as were mean chronic lethal minima of wildtype (5.3 °C, n=16$n=16$) and transgenic (5.6 °C, n=20$n=20$) zebra danios initially acclimated to 20 °C. These temperature tolerance values were used to estimate potential geographic distributions of the two varieties in the USA. Distributions of these D. rerio varieties in the USA should not be limited by their upper temperature tolerances, and low-temperature tolerance data suggest that both varieties are capable of overwintering in some southern and western US waters.     

Variations in piscivory of invasive largemouth bass <Emphasis Type="Italic">Micropterus salmoides</Emphasis> associated with pond environments

Introductions of non-native predatory fishes can be a major driver of aquatic biodiversity loss. The largemouth bass Micropterus salmoides (L.) has been introduced throughout much of the world, thereafter negatively affecting native faunal communities owing to its predatory impact. To investigate the environmental factors affecting the predatory performance of invasive bass, we examined the stomach contents and habitat characteristics of bass in 15 irrigation farm ponds in northeastern Japan. The food habits of the bass populations differed among the studied ponds: the predominant prey items were fishes among bass in seven of the ponds, whereas aquatic invertebrates (mainly insects and zooplankton) were the predominant taxa in the diets of bass in the eight remaining ponds, with the onset of piscivory related to body size. The results of multivariate analysis indicated that the extent to which the bass consumed fish was positively associated with fish prey abundance and negatively associated with percentage of aquatic vegetation coverage. We suggest that the extent of aquatic vegetation coverage strongly influenced the predation efficiency of bass in the ponds. These findings might be employed to assess a pond ecosystem’s vulnerability to invasive largemouth bass and to reduce the predator’s impact on native fish species by improvements to the habitat.     

Teasing apart crypsis and aposematism – evidence that disruptive coloration reduces predation on a noxious toad

Both cryptic and aposematic colour patterns can reduce predation risk to prey. These distinct strategies may not be mutually exclusive, because the impact of prey coloration depends on a predator's sensory system and cognition and on the environmental background. Determining whether prey signals are cryptic or aposematic is a prerequisite for understanding the ecological and evolutionary implications of predator–prey interactions. This study investigates whether coloration and pattern in an exceptionally polymorphic toad, Rhinella alata, from Barro Colorado Island, Panama reduces predation via background matching, disruptive coloration, and/or aposematic signaling. When clay model replicas of R. alata were placed on leaf litter, the model's dorsal pattern – but not its colour – affected attack rates by birds. When models were placed on white paper, patterned and un‐patterned replicas had similar attack rates by birds. These results indicate that dorsal patterns in R. alata are functionally cryptic and emphasize the potential effectiveness of disruptive coloration in a vertebrate taxon.     

DNA metabarcoding for dietary analysis of Holland's carp (Spinibarbus hollandi) to evaluate the threat to native fishes in Taiwan

DNA metabarcoding analysis for gut contents has been shown to compensate the disadvantage of traditionally morphological identification and offer higher resolution of prey items in an efficient way. Holland's carp (Spinibarbus hollandi) is a freshwater fish native to southern and eastern Taiwan. In the past two decades, this species has been introduced as a sport fish into the river basins of northern and western Taiwan. The large body size and active predation make it a potential threat for native fishes, but which native species are preyed by Holland's carp remains unknown. In this study, the diet from the gut contents of Holland's carp from the Zhonggang River, an invaded basin, was examined using DNA metabarcoding from 51 individuals and by morphological examinations on 140 samples. Detritus of plants were found in 83.6% samples (117 individuals). Twenty fish species of seven families were identified by DNA metabarcoding, including species of all water layers. Taiwan torrent carp (Acrossocheilus paradoxus) and Rhinogobius spp. are the most common prey items. Based on the results of this study, Holland's carp is considered an opportunistic omnivore because of its diverse diet items, which is an important trait for successful invasive fish species. The population decline of Opsariichthys pachycephalus may not result from the invasion of Holland's carps. Nonetheless, the time lag between successful invasion and the samplings of this study may be a concern because the population size of O. pachycephalus may have declined and become difficult to prey. The Holland's carps consumed the least species in winter; nonetheless, the occurrence frequencies of preys among seasons were not significantly different probably because of limited temperature fluctuation. The smallest Holland's carps consumed the least prey species compared to other size categories, similar to the relationship of prey species number to size of invasive largemouth bass (Micropterus salmoides).     

Predator naïve minnows respond to their conspecific alarm substance but not the odour from a non-native predator

When exposed to predator cues, ostariophysan fishes exhibit short-term anti-predator behavioural responses in order to minimise predation risk. Non-native predator cues are, however, likely to elicit poor behavioural responses in native prey fishes. This study investigated whether chubbyhead barb Enteromius anoplus, a native freshwater minnow in South Africa, had the innate ability to recognise and respond to largemouth bass Micropterus salmoides, a non-native piscivore. This was experimentally evaluated by investigating behavioural responses to both the non-native predator's odour and damage-released conspecific alarm substance (CAS). Chubbyhead barbs did not exhibit any behavioural response to largemouth bass odour both before and after exposure to CAS. This suggests that the chubbyhead barbs likely lacked the innate ability to recognise the non-native largemouth bass predator kairomones. By comparison, exposure to CAS was associated with significant behavioural responses, with chubbyhead barbs shifting from free-swimming to hovering, and frequent use of refugia. This suggests that despite ineffective response to non-native largemouth bass odour, chubbyhead barbs responded to general predator attack. Overall, this study suggests the potential for non-native largemouth bass to induce negative consumptive effects on chubbyhead barbs due to their inability to identify non-native predator's odour. In addition, nonconsumptive effects are likely due to altered activities in response to predator attack.     

The influence of littoral zone coarse woody habitat on home range size, spatial distribution, and feeding ecology of largemouth bass (Micropterus?salmoides)

Coarse woody habitat (CWH) may be a critical feature of lakes that influences fish distributions, movement patterns, and feeding habits. We used radio telemetry to examine the role of CWH in determining the movements of largemouth bass (Micropterus salmoides Lacepede) in the context of two whole-lake experiments that provided a gradient of four lake basins varying in natural and manipulated CWH. We also conducted diet studies on largemouth bass in these lakes to test for correlates among consumption rate and prey selectivity with bass behavior. Our results indicated that largemouth bass in basins with lower CWH abundances had larger home ranges, spent more time in deep water, were more selective predators, and showed lower consumption rates. Largemouth bass in basins with higher CWH abundances showed the opposite patterns. Low CWH abundances were correlated with a shift in largemouth bass foraging behavior from sit-and-wait to actively searching. This increased activity, coupled with the potential decline of prey fish species in the absence of CWH, may decrease largemouth bass growth potential regardless of the prey type consumed. Our results suggest that lakeshore residential development and associated removals of CWH from lakes may influence fish behavior, while CWH augmentation may reverse some of those changes. Handling editor: Steven Declerck     

An avoidance learning submodel for a general predation model

Summary This paper attempts to determine the effect on the number of prey eaten by predators of the addition of the component avoidance learning by prey to a computer model of the predation process developed by Holling. Generality was retained by concentrating upon a basic aspect of the prey's behaviour, its distance of reaction to an approaching predator. The zebra danio (Brachydanio rerio), a small freshwater fish, was used as an analogue of a general vertebrate prey. The predator used was the largemouth bass (Micropterus salmoides).Previous work (Dill, 1973b) showed that prey reactive distance increased with increasing experience with the predator. In the present study, this increased prey reactive distance is shown to increase predator pursuit time and hypothesized to decrease predator pursuit success. These relationships were expressed mathematically and built into Holling's (1965, 1966) model of the predation process, along with an equation describing the way in which reactive distance increases following an unsuccessful attack. Other changes necessitated in the model by the addition of the avoidance learning component included: a) Modifications of the calculation of search time to remove a previously implicit time spent unsuccessfully pursuing prey, and to correct the density of prey to account for those whose reactive distances exceed that of the predator and are therefore not susceptible to discovery; b) Addition of a new subroutine (CHASE) to calculate pursuit time, unsuccessful pursuit time, pursuit success, and strike success; c) Changes in subroutine ADCOM to assign prey to different classes (with different reactive distances) according to the number of times they have been unsuccessfully attacked; and d) Addition of a stochastic element via random numbers to determine the class to which an attacked prey belongs, the time to refuge, and the predator's strike success.Simulation was used to explore the consequences of these additions. The capability of learning substantially increased the prey's probability of surviving subsequent attack. Addition of an avoidance learning component caused declines in the predator's functional responses to both prey and predator density. The new component was also suggested to decrease the predator's numerical response to prey density and to increase the probability of stability in a predator-prey interaction.From a thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy, University of British Columbia.     

Eurasian otter (<Emphasis Type="Italic">Lutra lutra</Emphasis>) diet and prey selection in Mediterranean streams invaded by centrarchid fishes

The diet of the Iberian otter (Lutra lutra) was determined by analysing 547 spraints collected at 28 sites within a wide area invaded by centrarchid fishes (pumpkinseed sunfish, Lepomis gibbosus and largemouth bass, Micropterus salmoides): the middle Guadiana basin (South-west Iberian Peninsula). Fish was the otters’ main prey, representing more than 60% of total individuals and more than 80% of total biomass. Otters preyed on most of the fish species captured in the field; however, the consumption of centrarchids was low compared to their abundance in the streams, and Jacobs’ index of preference showed a clear rejection of both species by the otter. Consumption of native fish genera (Squalius, Barbus and Chondrostoma) by otters increased in relation to their increase in the environment. In contrast, increasing numbers of L. gibbosus in the field was not reflected in otter consumption. The general decline of native freshwater fishes in Iberian rivers, the preferred prey of otters, together with the spread of exotic fish species (centrarchids and others) could put otter populations at risk.     

Invasive carp and prey community composition disrupt trophic cascades in eutrophic ponds

The role of trophic cascades in structuring freshwater communities has been extensively studied. Most of this work, however, has been conducted in oligotrophic northern lakes that contain highly vulnerable cyprinid prey: aquatic communities where trophic interactions are likely to be stronger than in many other systems. Fewer studies have been conducted in eutrophic systems or have examined the bottom-up effects of benthivorous fishes, and none have directly compared these effects to those of piscivores on ecosystem structure and function. We conducted enclosure experiments in eutrophic ponds to examine trophic effects of invasive benthivores (common carp—Cyprinus carpio L.), native piscivores (largemouth bass—Micropterus salmoides [Lacepède]), and their interactions with common centrarchid prey with well-developed anti-predatory behaviors (age-1 bluegill—Lepomis macrochirus Rafinesque and young-of-year largemouth bass). At the end of the 60-day experiment, common carp had strong bottom-up effects that increased total phosphorus and turbidity while decreasing chlorophyll a biomass and macrophyte cover that resulted in decreased macroinvertebrate biomass and also decreased growth in both juvenile largemouth bass and bluegill. Piscivorous largemouth bass, however, did not affect the survival of either planktivorous juvenile largemouth bass or bluegill. Growth of juvenile largemouth bass was also not affected, but juvenile bluegill growth was significantly diminished, possibly due to nonconsumptive effects of predation. Our results suggest that, in a centrarchid-dominated eutrophic system, top-down effects of predators are overwhelmed by common carp-mediated bottom-up effects. These bottom-up effects strongly affected multiple trophic levels, thus altering aquatic community structure and function.     

Experienced chicks show biased avoidance of stronger signals: an experiment with natural colour variation in live aposematic prey

An important factor for understanding the evolution of warning coloration in unprofitable prey is the synergistic effect produced by predator generalisation behaviour. Warning coloration can arise and become stabilised in a population of solitary prey if more conspicuous prey benefit from a predator's previous interaction with less conspicuous prey. This study investigates whether domestic chicks (Gallus gallus domesticus) show a biased generalisation among live aposematic prey by using larvae of three species of seed bugs (Heteroptera: Lygaeidae) that are of similar shape but vary in the amount of red in the coloration. After positive experience of edible brownish prey, chicks in two reciprocal experiments received negative experience of either a slightly red or a more red distasteful larva. Attacking birds were then divided into two treatment groups, – one presented with the same prey again, and one presented with either a less red or a more red larva. Birds with only experience of edible prey showed no difference in attack probability of the two aposematic prey types. Birds with experience of the less red prey biased their avoidance so that prey with a more red coloration was avoided to a higher degree, whereas birds with experience of the more red prey avoided prey with the same, but not less red coloration. Thus, we conclude that bird predators may indeed show a biased generalisation behaviour that could select for and stabilise an aposematic strategy in solitary prey. This revised version was published online in July 2006 with corrections to the Cover Date.     

The effects of predator learning, forgetting, and recognition errors on the evolution of warning coloration

This paper demonstrates that the specifics of predator avoidance learning, information loss, and recognition errors may heavily influence the evolution of aposematism. I establish a mathematical model of the change in frequency over time of bright individuals of a distasteful prey species. Warning color spreads through green beard selection as reformulated by Guilford (1990); bright colored forms gain an advantage due to their phenotypic resemblance to other bright forms, which have been sampled by the predator. I use a general classical conditioning model to examine gradual predator learning and forgetting, and then consider the extreme of one-trial learning and no forgetting over time that may occur with very toxic prey. The advantage of conspicuous coloration under these latter conditions depends upon its role in lowering a constant probability of the prey being misidentified and thus mistakenly attacked by a predator, a rarely emphasized factor in the evolution of warning coloration. This constant probability of mistaken attacks can also be interpreted as a constant probability that forgetting has occurred (forgetting does not increase with time) or a periodic decision by the predator to resample avoided prey. I show that when predators learn and forget gradually, as under the general classical conditioning model, it is very difficult for aposematic coloration to become established unless bright individuals cross an often high threshold frequency through chance factors. In contrast, the conditions expected with highly toxic prey promote the evolution of warning coloration more easily, by means from the fixation of very bright mutations to the fixation of successive mutations each of which causes a small increase in a prey's conspicuousness. The results therefore predict that aposematic coloration may have evolved in a different manner in different predator and prey systems. They also suggest that it may be extremely difficult for warning coloration to evolve in more mildly toxic or distasteful prey outside of a mimicry system.     

Effects of crayfish size,orientation, and movement on the reactive distance of largemouth bass foraging in clear and turbid water

Laboratory experiments were performed in clear and turbid water to determine the effects of prey size, orientation, and movement on the reactive distance of largemouth bass (Micropterus salmoides) when feeding on crayfish (Procambarus acutus). In clear water, the reactive distance increased linearly with an increase in prey size, and prey movement resulted in a significant increase in the reactive distance. Prey orientation (head-on versus perpendicular) did not change the reactive distances. In moderately turbid water, the reactive distance did not increase with increased prey size, and prey movement did not result in any changes in the reactive distance. The absence of any effects of prey orientation in clear water or prey movement in turbid water is inconsistent with results from studies using different species (primarily planktivorous fish). I propose that largemouth bass change their foraging tactics as prey visibility changes. When prey are highly visible (low turbidity), predators attack (react) only after prey recognition, which is based on multiple cues such as prey size (length, width) and movement. When prey are less visible (high turbidity), predators attack immediately upon initial prey sighting, which does not depend on prey size or movement.     

The Influence of Alarm Substance on Feeding in Zebra Danio Fish (Brachydanio rerio)

The effects of alarm substance on feeding behaviour of zebra danio fish (Brachydanio rerio) were tested by offering them high and low densities of enclosed waterfleas (Daphnia magna). Normally the fish attacked high densities of prey, but when exposed to alarm substance they preferred lower and presumably less confusing prey densities — also lowering their feeding rate.     

The diet of largemouth bass, Micropterus salmoides, in Lake Naivasha, Kenya

Lake Naivasha is a freshwater lake situated in the eastern rift valley of Kenya. Only five species of fish are present, all of which have been introduced. Of these, Oreochromis leucostictus, Tilapia zillii and Micropterus salmoides (largemouth black bass) support an important gillnet fishery with bass also being taken for sport. Until bass reached 260 mm f.l. they depended upon invertebrate food organisms. Thereafter crayfish, fish and frogs became increasingly important the larger the size of the bass. The most important invertebrate prey species was the water boatman, Micronecta scutellaris , followed by chironomid and culicid pupae. Zooplank-ton was consumed but only in large quantity by fish smaller than 80 mm. For bass over 260 mm the crayfish, Procambarus darkii , was the principal food. The largemouth bass in Lake Naivasha are generalized macro-predators, feeding principally on free-living animals of a kind most likely to be found in the littoral zones.     

The interplay between multiple predators and prey colour divergence

Evolutionary divergence in the coloration of toxic prey is expected when geographic variation in predator composition and behavior favours shifts in prey conspicuousness. A fundamental prediction of predator‐driven colour divergence is that the local coloration should experience lower predation risk than novel prey phenotypes. The dorsal coloration of the granular poison frog varies gradually from populations of conspicuous bright red frogs to populations of dull green and relatively cryptic frogs. We conducted experiments with clay models in four populations to examine the geographic patterns of taxon‐specific predation. Birds avoided the local phenotype while lizards consistently selected for decreased conspicuousness and crab predation did not depend on frog coloration. Importantly, birds and lizards favoured low conspicuousness in populations where relatively cryptic green morphs have evolved. This study provides evidence for the interplay among distinct selective pressures, from multiple‐predator taxa, acting on the divergence in protective coloration of prey species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 580–589.     

Honest signaling and the uses of prey coloration

Abstract Although signal reliability is of fundamental importance to the understanding of animal communication, the extent of signal honesty in relation to antipredator warning signals has received relatively little attention. A recent theoretical model that assumed a physiological linkage between pigmentation and toxicity suggested that (aposematic) warning signals may often be reliable, in the sense that brightness and toxicity are positively correlated within prey populations. Two shortcomings of the model were (1) the requirement among predators for an innate aversion to brightly colored prey and (2) the assumption that prey can generate only bright coloration and not cryptic coloration. We evaluated the generality of predictions of reliable signaling when these shortcomings were removed. Without innate avoidance of bright prey, we found a positive brightness-toxin correlation when conspicuous prey coloration provided an additional fitness benefit unrelated to predation. Initially, this correlation could evolve for reasons unrelated to prey signaling; hence, aposematism might represent a striking example of exaptation. Given a choice between using pigmentation for bright or for cryptic coloration, crypsis was favored only in conditions of very low or very high resource levels. In the latter case, toxicity correlated positively with degree of cryptic coloration. Predictions of toxin-signal correlation appear robust, but we can identify interesting conditions in which signal reliability is not predicted.