Variation in growth and age at maturity in bluegill sunfish: genetic or environmental effects?

Populations of bluegill sunfish Lepomis macrochirus , experiencing heavy juvenile predation, showed increased growth rates and increased age and size at maturity relative to populations experiencing decreased predation on juveniles but increased predation on adults. This study examined bluegills experimentally from both types of populations and a cross between them in a common environment to determine if variation in growth and age at maturity is genetically or environmentally induced. Two factorial experiments, varying strain of bluegills and resource availability, were used to evaluate differences in growth rate. One experiment, varying strain of bluegills, was used to assess differences in age at maturity. Growth was strongly influenced by resource level, but growth rate did not vary among populations. Nearly all bluegills in each population matured at 1 year of age in a common environment. Thus, variation observed in source populations must be mostly attributable to differences in the environment between populations. At least three factors could potentially cause differences in growth and age at maturity: (1) variation in resource availability; (2) variation in demographic structure; and (3) variation in size-specific mortality rates caused by differences in predator abundance between populations. Observed patterns of variation between populations are best explained by effects of differences in predator populations.     

Phenotypic variation and vulnerability to predation in juvenile bluegill sunfish (<Emphasis Type="Italic">Lepomis macrochirus</Emphasis>)

Bluegill sunfish (Lepomis macrochirus) are known to diversify into two forms specialized for foraging on either limnetic or littoral prey. Because juvenile bluegills seek vegetative cover in the presence of largemouth bass (Micropterus salmoides) predators, natural selection should favor the littoral body design at size ranges most vulnerable to predation. Yet within bluegill populations, both limnetic and littoral forms occur where vegetation and predators are present. While adaptive for foraging in different environments, does habitat-linked phenotypic variation also influence predator evasiveness for juvenile bluegills? We evaluate this question by quantifying susceptibility to predation for two groups of morphologically distinct bluegills; a limnetic form characteristic of bluegills inhabiting open water areas (limnetic bluegill) and a littoral form characteristic of bluegills inhabiting dense vegetation (littoral bluegill). In a series of predation trials, we found that bluegill behaviors differed in open water habitat but not in simulated vegetation. In open water habitat, limnetic bluegills formed more dense shoaling aggregations, maintained a larger distance from the predator, and required longer amounts of time to capture than littoral bluegill. When provided with simulated vegetation, largemouth bass spent longer amounts of time pursuing littoral bluegill and captured significantly fewer littoral bluegills than limnetic fish. Hence, morphological and behavioral variation in bluegills was linked to differential susceptibility to predation in open water and vegetated environments. Combined with previous studies, these findings show that morphological and behavioral adaptations enhance both foraging performance and predator evasiveness in different lake habitats.     

Behavioural Response of Juvenile Bluegill Sunfish to Variation in Predation Risk and Food Level

The behavioural response of juvenile bluegill sunfish (Lepomis macrochirus) to predation risk when selecting between patches of artificial vegetation differing in food and stem density was investigated. Bluegill foraging activity was significantly affected by all three factors. Regardless of patch stem density or risk of predation bluegills preferred patches with the highest prey number. During each trial bluegill foraging activity was clearly divided into a between- and within-patch component. In the presence of a predator bluegills reduced their between-patch foraging activity by an equivalent amount regardless of patch stem density or food level, apparently showing a risk-adjusting behavioural response to predation risk. Within patches, however, foraging activity was affected by both food level and patch stem density. When foraging in a patch offering a refuge from predation, the presence of a predator had no effect on bluegill foraging activity within this patch. However, if foraging in a patch with only limited refuge potential, bluegill foraging activity was reduced significantly in the presence of a predator. Further, this reduction was significantly greater if the patch contained a low versus a high food level, indicating a risk-balancing response to predation with respect to within-patch foraging activity. Both these responses differ from the risk-avoidance response to predation demonstrated by juvenile bluegills when selecting among habitats. Therefore, our results demonstrate the flexibility of juvenile bluegill foraging behaviour.     

Variation in plant stem density and its effects on foraging success of juvenile bluegill sunfish

Synopsis Juvenile bluegill sunfish, Lepomis macrochirus, are known to use beds of aquatic vegetation as a refuge from predators. This study examines the effects of increasing plant stem density on juvenile bluegill foraging. Three stem densities (100, 250 and 500 stems m⁻²), varying in their refuge potential for bluegills from predators, were tested. Results demonstrate that stem densities chosen as a refuge from predation (i.e. 500 stems m⁻²) significantly reduced bluegill foraging success and increased time required to capture prey. Therefore, juvenile bluegills seeking safety in vegetation may be faced with a trade-off between foraging success and effective refuge from predation when choosing among plant stem densities.     

How light, a predator, and experience influence bluegill use of shade and schooling

Bluegills, Lepomis macrochirus, form schools and use shade to avoid predators. How light intensity, predators, and experience might affect antipredator behavior of bluegill are not well understood. Hence, we evaluated use of shade and schooling by naive (hatchery) and experienced (wild) bluegills (50–60 mm total length) at four light levels (1.5, 85, 169, 340 lux) in the presence and absence of a model predator in experimental pools. Naive bluegills used shade extensively at all light levels, even when the predator was in the shade. They rarely schooled, preferring to shoal in the shade. Experienced bluegill used shade when the predator was in the open and avoided shade when the predator was there. Schooling was more prevalent at low light levels when shade was less intense. Use of shade became an increasingly important behavior at higher light levels, unless the predator was in the shade. A shaded predator caused experienced bluegills to shoal tightly in the opposite, open area. These data suggest naive bluegills may not have considered the model predator a threat. Their behavior suggests avian predator avoidance, a possibility given that avian predators were present at the hatchery. Experienced bluegill employed behaviors that would be useful in avoiding piscine predators.     

Using Environmental DNA to Estimate the Distribution of an Invasive Fish Species in Ponds

Knowledge of the presence of an invasive species is critical to monitoring the sustainability of communities and ecosystems. Environmental DNA (eDNA), DNA fragments that are likely to be bound to organic matters in the water or in shed cells, has been used to monitor the presence of aquatic animals. Using an eDNA-based method, we estimated the presence of the invasive bluegill sunfish, Lepomis macrochirus, in 70 ponds located in seven locales on the Japanese mainland and on surrounding islands. We quantified the concentration of DNA copies in a 1 L water sample using quantitative real-time polymerase chain reaction (qPCR) with a primer/probe set. In addition, we visually observed the bluegill presence in the ponds from the shoreline. We detected bluegill eDNA in all the ponds where bluegills were observed visually and some where bluegills were not observed. Bluegills were also less prevalent on the islands than the mainland, likely owing to limited dispersal and introduction by humans. Our eDNA method simply and rapidly detects the presence of this invasive fish species with less disturbance to the environment during field surveys than traditional methods.     

Predator-mediated habitat use: some consequences for species interactions

Synopsis Behavioral responses to predators can have a major impact on a fishes' diet and habitat choice. Studies with the bluegill sunfish, Lepomis macrochirus, demonstrate that bluegills undergo pronounced shifts in diet and habitat use as they grow in response to changes in their vulnerability to predators. Other species of fish exhibit similar habitat shifts with body size, presumably also in response to changing predation risks and/or foraging gains. An important but little appreciated consequence of this type of predator-mediated habitat use is that predation risk, by structuring size and/or age-specific resource use, may also indirectly affect species interactions. This paper discusses some of the ways in which behavioral responses to predators may affect intra- and interspecific competition in fish. Observational and experimental studies with sunfish (Centrarchidae) provide most of the examples. These studies suggest that the nonlethal effects of predators may be as important as the actual killing of prey.     

Plant stem density as a cue in patch choice by foraging juvenile bluegill sunfish

Synopsis Juvenile bluegill sunfish,Lepomis macrochira, are restricted to vegetated habitats by predators. Variation in plant stem density has a significant effect on bluegill foraging success. Given the mosaic nature of this habitat, plant stem density may provide a cue for selecting among patches in which to forage. In this study, juvenile bluegills were offered patches of artificial vegetation differing only in plant stem density as potential foraging sites. Three densities, 100, 250, and 500 stems m^–2 were tested. Fish were presented with a choice between patches (100:250, 250:500, or 100:500). Bluegill foraging rate in, and the number of fish choosing each patch was recorded. Juvenile bluegills showed a preference for those patches which maximized their foraging rate.     

Predator avoidance,microhabitat shift,and risk-sensitive foraging in larval dragonflies

Summary Dragonfly larvae (Odonata: Anisoptera) are often abundant in shallow freshwater habitats and frequently co-occur with predatory fish, but there is evidence that they are underutilized as prey. This suggests that species which successfully coexist with fish may exhibit behaviors that minimize their risk of predation. I conducted field and laboratory experiments to determine whether: 1) dragonfly larvae actively avoid fish, 2) microhabitat use and foraging success of larvae are sensitive to predation risk, and 3) vulnerability of larvae is correlated with microhabitat use. I experimentally manipulated the presence of adult bluegills (Lepomis macrochirus) in defaunated patches of littoral substrate in a small pond to test whether colonizing dragonfly larvae would avoid patches containing fish. The two dominant anisopteran species, Tetragoneuria cynosura and Ladona deplanata (Odonata: Libellulidae), both strongly avoided colonizing patches where adult bluegills were present. Laboratory experiments examined the effects of diel period and bluegills on microhabitat use and foraging success, using Tetragoneuria, Ladona and confamilial Sympetrum semicictum, found in a nearby fishless pond. Tetragoneuria and Ladona generally occupied microhabitats offering cover, whereas Sympetrum usually occupied exposed locations. Bluegills induced increased use of cover in all three species, and use of cover also tended to be higher during the day than at night. Bluegills depressed foraging in Tetragoneuria and to a lesser extent in Ladona, but foraging in Sympetrum appeared unaffected. Other laboratory experiments indicated that Sympetrum were generally more vulnerable than Tetragoneuria or Ladona to bluegill predation, and that vulnerability was positively correlated with use of exposed microhabitats. Both fixed (generally low use of exposed microhabitats, diel microhabitat shifts) and reactive (predator avoidance, predator-sensitive microhabitat shifts) behavioral responses appear to reduce risk of predation in dragonfly larvae. Evidence indicates that vulnerability probably varies widely among species and even among instars within species, and suggests that spatial distributions of relatively vulnerable species may be limited by their inability to avoid predation.     

A peculiar relationship between genetic diversity and adaptability in invasive exotic species: bluegill sunfish as a model species

A peculiar relationship exists between population genetics and invasion biology. Introduced populations often suffer a depletion of genetic variation, but they can persist and adapt to new environments. Here, we show that this relationship is observed in bluegill sunfish (Lepomis macrochirus), an invasive exotic fish in Japan. Genetic analysis using selectively neutral genetic markers reconfirmed that the bluegill introduced into Japan from the United States in 1960 had a single origin with only 15 founders. The analysis also shows that in the process of range expansion, the introduced bluegills experienced severe depletion of genetic diversity due to the founder effect and/or genetic drift. Despite such a decline in genetic diversity, the bluegill populations exhibited a divergent feeding morphology in response to the colonized environments. Such a morphological divergence can facilitate prey exploitation, thereby causing a greater negative impact on native prey resources. Further, in a trophically polymorphic bluegill population in Lake Biwa, physiological characteristics and genetic structures of the intestinal bacterial communities were associated with the difference in diet among the trophic morphs in the host bluegill population. This empirical evidence suggests that despite the severe decline in genetic diversity, the introduced bluegill populations rapidly adapted to the new environment and formed diverse functional relationships with the native bacterial community. Thus, these findings suggest that genetic variation at selectively neutral markers does not always predict adaptability and invasiveness in introduced populations.     

Community structure and seasonal dynamics of helminth parasites in Lepomis cyanellus and L. macrochirus from Charlie's Pond, North Carolina: host size and species as determinants of community structure

The community structure and seasonal dynamics of 16 helminth species infecting green (Lepomis cyanellus) and bluegill (L. macrochirus) sunfishes in Charlie's Pond, North Carolina, was examined. One hundred and fifty-four fishes including 90 green sunfish and 64 bluegill sunfish were collected between March and November 2000 and examined for the presence of helminth parasites. Five of these species underwent significant changes in abundance in green sunfish infracommunities, 3 of which also displayed seasonal changes in prevalence. Three of the 16 species fluctuated seasonally in bluegill infrapopulations; 2 also underwent changes in prevalence. Species richness and diversity varied across the 9-mo period for both host species, whereas total helminth abundance remained constant. Analysis of component communities revealed differences in community structure for the 2 host species. Bluegills were found to harbor larger and more diverse communities. Bluegills also contained larger infrapopulations of 5 species, whereas green sunfish had greater abundance of 2 species. Interpretation of these data suggests that host species and size are strongly associated with the predictability of community structure.     

Spatial and Temporal Trade-Offs by Bluegills in Floodplain River Ecosystems

Ecological trade-offs by organisms to minimize mortality and maximize growth is a foundational theme in ecology. Yet, these trade-offs are rarely examined within spatially complex, temporally variable ecosystems, such as floodplain rivers. Here, we evaluate ecological trade-offs across space and time for the bluegill (Lepomis macrochirus) in two unregulated river ecosystems in southeastern USA. Life-history differences among spatially segregated main channel and floodplain lake populations were used to assess effects of habitat type on bluegill fitness. Growth, condition, and gonadal somatic index were all significantly enhanced in floodplain lakes relative to the main channel. Furthermore, stomach fullness was significantly higher, and predator densities significantly lower in floodplain lakes thereby providing an ecological explanation for the life-history plasticity observed across the riverscape. However, historical observations suggested that although floodplain lakes are highly productive for bluegills, they are also prone to complete desiccation by drought approximately every 5 years, revealing the ultimate value of channel habitat, which does not dry, as desiccation refugia. Bluegills are faced with a balancing act associated with variation in foraging opportunities, and risks to predation and desiccation, that change in both the temporal and the spatial dimensions of floodplain rivers. The differential responses to these opportunities and risks help to explain why both habitats remain actively populated by bluegills, as well as many other organisms, in these and many other natural rivers.     

Adaptive life-history evolution in the livebearing fish Brachyrhaphis rhabdophora: genetic basis for parallel divergence in age and size at maturity and a test of predator-induced plasticity

I document a genetic basis for parallel evolution of life-history phenotypes in the livebearing fish Brachyrhaphis rhabdophora from northwestern Costa Rica. In previous work, I showed that populations of B. rhabdophora that co-occur with predators attain maturity at smaller sizes than populations that live in predator-free environments. I also demonstrated that this pattern of phenotypic divergence in life histories was independently repeated in at least five isolated drainages. However, life-history phenotypes measured from wild-caught fish could be attributed to environmental effects rather than to genetic differences among populations. In the present study, I reared male fish from four populations (two that co-occur with predators and two from predator-free environments) under four sets of environmental conditions. The pattern of phenotypic divergence in maturation size documented in the field between populations collected from different predation environments persisted after two generations in the laboratory. I also found a genetic basis for differences between populations in the age at which males attain maturity and in growth rates. By rearing fish in four different common environments, I tested for phenotypic plasticity in male life-history traits in response to nonlethal exposure to predators. There was a significant delay in the onset of sexual maturity in fish exposed to predators relative to those in the control, but no differences among treatments in size at maturity or growth rates. These results, coupled with previous work on B. rhabdophora, demonstrate a repeated pattern of parallel evolutionary divergence among genetically isolated populations that is strongly associated with predation.     

Bluegill growth as modified by plant density: an exploration of underlying mechanisms

Summary Bluegill (Lepomis macrochira) growth varies inconsistently with plant density. In laboratory and field experiments, we explored mechanisms underlying bluegill growth as a function of plant and invertebrate density. In the laboratory, bluegills captured more chironomids (Chironomus riparius) than damselflies (Enallagma spp. and Ischnura spp.), but energy intake per time spent searching did not differ between damselfly and chironomid treatments. From laboratory data, we described prey encounter rates as functions of plant and invertebrate density. In Clark Lake, Ohio, we created 0.05-ha mesocosms of inshore vegetation to generate macrophyte densities of 125, 270, and 385 stems/m² of Potamogeton and Ceratophyllum and added 46-mm bluegill (1/m²). In these mesocosms, invertebrate density increased as a function of macrophyte density. Combining this function with encounter rate functions derived from laboratory data, we predicted that bluegill growth should peak at a high macrophyte density, greater than 1000 stems/m², even though growth should change only slightly beyond 100 stems/m². Consistent with our predictions, bluegills did not grow differentially, nor did their use of different prey taxa differ, across macrophyte densities in the field. Bluegills preferred chironomid pupae, which were relatively few in numbers but vulnerable to predation, whereas more cryptic, chironomid larvae, which were associated with vegetation but were relatively abundant, were eaten as encountered. Bluegills avoided physid snails, which were abundant. Contrary to previous work, vegetation did not influence growth or diet of bluegill beyond relatively low densities owing to the interaction between capture probabilities and macroinvertebrate densities.The unit is sponsored jointly by the United States Fish and Wildlife Service, Ohio Department of Natural Resources, The Ohio State University, and The Wildlife Management Institute     

Selective predation,parasitism, and trophic cascades in a bluegill–<Emphasis Type="Italic">Daphnia</Emphasis>–parasite system

As disease incidence increases worldwide, there is increased interest in determining the factors controlling parasitism in natural populations. Recently, several studies have suggested a possible role of predation in reducing parasitism, but this idea has received little experimental attention. Here, I present the results of an experiment in which I manipulated predation rate in large field enclosures to test the effects of predation on parasitism using a bluegill predator–Daphnia host–yeast parasite system. Based on previous work showing high bluegill sunfish selectivity for infected over uninfected Daphnia, I anticipated that predators would reduce infection levels. Contrary to expectations, predation did not reduce infection prevalence. Instead, there were large epidemics in all treatments, followed by reductions of host density to very low levels. As Daphnia density decreased, phytoplankton abundance increased and water clarity decreased, suggesting a parasite-driven trophic cascade. Overall, these results suggest that selective predation does not always reduce infection prevalence, and that parasites have the potential to drastically reduce host densities even in the presence of selective predators. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Chemical cues from multiple predator-prey interactions induce changes in behavior and growth of anuran larvae

Chemical signals are used as information by prey to assess predation risk in their environment. To evaluate the effects of multiple predators on prey growth, mediated by a change in prey activity, I exposed small and large bullfrog (Rana catesbeiana) larvae (tadpoles) to chemical cues from different combinations of bluegill sunfish (Lepomis macrochirus) and larval dragonfly (Anax junius) predators. Water was regularly transferred from predation trials (outdoor experiment) to aquaria (indoor experiment) in which activity and growth of tadpoles was measured. The highest predation mortality of small bullfrog larvae in the outdoor experiment was due to Anax, and it was slightly lower in the presence of both predators, probably resulting from interactions between predators. There was almost no mortality of prey with bluegill. The activity and growth of small bullfrog larvae was highest in the absence of predators and lowest in the presence of Anax. In the presence of bluegill only, or with both predators, the activity and growth of small bullfrog tadpoles was intermediate. Predators did not affect large tadpole activity and growth. Regressing mortality of small bullfrog tadpoles against activity and growth of bullfrog tadpoles revealed a significant effect for small bullfrog larvae but a non-significant effect for large bullfrog larvae. This shows that the response of bullfrog tadpoles to predators is related to their own body size. The experiment demonstrates that chemical cues are released both as predator odor and as alarm substances and both have the potential to strongly alter the activity and growth of prey. Different mechanisms by which chemical cues may be transmitted to species interactions in the food web are discussed. Received: 28 June 1999 / Accepted: 15 November 1999     

LOCAL ADAPTATION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY IN TRINIDADIAN GUPPIES (POECILIA RETICULATA)

Divergent selection pressures across environments can result in phenotypic differentiation that is due to local adaptation, phenotypic plasticity, or both. Trinidadian guppies exhibit local adaptation to the presence or absence of predators, but the degree to which predator‐induced plasticity contributes to population differentiation is less clear. We conducted common garden experiments on guppies obtained from two drainages containing populations adapted to high‐ and low‐predation environments. We reared full‐siblings from all populations in treatments simulating the presumed ancestral (predator cues present) and derived (predator cues absent) conditions and measured water column use, head morphology, and size at maturity. When reared in presence of predator cues, all populations had phenotypes that were typical of a high‐predation ecotype. However, when reared in the absence of predator cues, guppies from high‐ and low‐predation regimes differed in head morphology and size at maturity; the qualitative nature of these differences corresponded to those that characterize adaptive phenotypes in high‐ versus low‐predation environments. Thus, divergence in plasticity is due to phenotypic differences between high‐ and low‐predation populations when reared in the absence of predator cues. These results suggest that plasticity might initially play an important role during colonization of novel environments, and then evolve as a by‐product of adaptation to the derived environment.     

Interactions between adult and larval bluegill sunfish: positive and negative effects

Adult fish may affect the growth and survival of conspecific larvae through a variety of pathways, including negative interactions via competition for shared limiting resources or via predation (i.e., cannibalism), and positive interactions due to the consumption of larval predators and via resource enhancement (i.e., presence of adults increases availability of larval prey). To examine the overall effect of adult bluegill sunfish (Lepomis macrochirus) on larval bluegill, we conducted a field experiment in which we manipulated adult densities and quantified larval growth and survival, prey abundance, invertebrate predator abundance, and cannibalism. The presence of adult bluegill had a negative effect on final larval mass. This response was consistent with competition for zooplankton prey. Adult bluegill reduced the abundance of large zooplankton (e.g., Chaoborus and Daphnia), which were the dominant prey of bluegill larvae in the absence of adults. Larvae in the no-adult treatment also had significantly more prey in their stomachs compared to larvae in the presence of adults. Larval survival was maximized at intermediate adult densities and the overall production of larvae peaked at intermediate adult densities. The higher larval survival at intermediate adult densities is attributed to a reduction in invertebrate predators in treatments with adult bluegill; invertebrate predators experienced an 80% reduction in the presence of adult fish. Decreased larval survival at the highest adult density was not due to resource limitation and may be due to cannibalism, which was not directly observed in our study, but has been observed in other studies.     

Interactions of bullfrog tadpole predators and an insecticide: predation release and facilitation

The effect of a contaminant on a community may not be easily predicted, given that complex changes in food resources and predator-prey dynamics may result. The objectives of our study were to determine the interactive effects of the insecticide carbaryl and predators on body size, development, survival, and activity of tadpoles of the bullfrog (Rana catesbeiana). We conducted the study in cattle tank mesocosm ponds exposed to 0, 3.5, or 7.0 mg/l carbaryl, and no predators or two red-spotted newts (Notophthalmus viridescens), bluegill sunfish (Lepomis macrochirus), or crayfish (Orconectes sp.). Carbaryl negatively affected predator survival by eliminating crayfish from all ponds, and by eliminating bluegill sunfish from ponds exposed to the highest concentration of carbaryl; carbaryl exposure did not effect survival of red-spotted newts. Because crayfish were eliminated by carbaryl, bullfrogs were released from predation and survival was near that of predator controls at low concentrations of carbaryl exposure. High concentrations of carbaryl reduced tadpole survival regardless of whether predators survived carbaryl exposure or not. Presence of crayfish and newts reduced tadpole survival, while bluegill sunfish appeared to facilitate bullfrog tadpole survival. Presence of carbaryl stimulated bullfrog tadpole mass and development. Our study demonstrates that the presence of a contaminant stress can alter community regulation by releasing prey from predators that are vulnerable to contaminants in some exposure scenarios.Due to an error in the citation line, this revised PDF (published in December 2003) deviates from the printed version, and is the correct and authoritative version of the paper.     

Patterns of Fish Growth along a Residential Development Gradient in North Temperate Lakes

Residential development of lakeshores is expected to change a variety of key lake features that include increased nutrient loading, increased invasion rate of nonnative species, increased exploitation rates of fishes by anglers, and alteration of littoral habitats. All of these factors may alter the capacity of lakes to support productive native fish populations. Fourteen north temperate lakes were surveyed to examine how growth rates of two common fish species (bluegill sunfish, Lepomis macrochirus; largemouth bass, Micropterus salmoides) varied along a residential development gradient. Size-specific growth rates for both species were negatively correlated with the degree of lakeshore residential development, although this trend was not statistically significant for largemouth bass. On average, annual growth rates for bluegill sunfish were 2.6 times lower in heavily developed lakes than in undeveloped lakes. This effect of lakeshore development on fish growth was not size specific for bluegills between 60 and 140 mm in total length. An index of population production rate that accounted for both the size-specific growth rate and the size distribution of fishes showed that bluegill populations were approximately 2.3 times less productive in highly developed lakes than in undeveloped lakes. Our results suggest that extensive residential development of lakeshores may reduce the fish production capacity of aquatic ecosystems. Received 29 April 1999; Accepted 26 October 1999.