Intraspecific phenotypic variation in a fish predator affects multitrophic lake metacommunity structure

Contemporary insights from evolutionary ecology suggest that population divergence in ecologically important traits within predators can generate diversifying ecological selection on local community structure. Many studies acknowledging these effects of intraspecific variation assume that local populations are situated in communities that are unconnected to similar communities within a shared region. Recent work from metacommunity ecology suggests that species dispersal among communities can also influence species diversity and composition but can depend upon the relative importance of the local environment. Here, we study the relative effects of intraspecific phenotypic variation in a fish predator and spatial processes related to plankton species dispersal on multitrophic lake plankton metacommunity structure. Intraspecific diversification in foraging traits and residence time of the planktivorous fish alewife (Alosa pseudoharengus) among coastal lakes yields lake metacommunities supporting three lake types which differ in the phenotype and incidence of alewife: lakes with anadromous, landlocked, or no alewives. In coastal lakes, plankton community composition was attributed to dispersal versus local environmental predictors, including intraspecific variation in alewives. Local and beta diversity of zooplankton and phytoplankton was additionally measured in response to intraspecific variation in alewives. Zooplankton communities were structured by species sorting, with a strong influence of intraspecific variation in A. pseudoharengus. Intraspecific variation altered zooplankton species richness and beta diversity, where lake communities with landlocked alewives exhibited intermediate richness between lakes with anadromous alewives and without alewives, and greater community similarity. Phytoplankton diversity, in contrast, was highest in lakes with landlocked alewives. The results indicate that plankton dispersal in the region supplied a migrant pool that was strongly structured by intraspecific variation in alewives. This is one of the first studies to demonstrate that intraspecific phenotypic variation in a predator can maintain contrasting patterns of multitrophic diversity in metacommunities.     

Predator-induced plasticity does not alter the pathway from evolution to ecology among locally adapted populations of <Emphasis Type="Italic">Daphnia</Emphasis>

In the growing field of eco-evolutionary dynamics, evidence for an influence of rapid shifts in phenotype on ecological processes is accumulating, yet, the contributions of phenotypic plasticity versus genetic change to these observed ecological changes are unclear. In one of the best studied ecosystems in terms of eco-evolutionary dynamics, landlocked versus anadromous alewife (Alosa pseudoharengus) have caused strong evolutionary divergence in their key zooplankton prey (Daphnia ambigua). We previously showed that such evolutionary differences have cascading ecological effects on consumer-resource dynamics and primary production. Yet, these locally adapted populations of Daphnia also differ in trait plasticity, which may, in turn, modify the pathway from evolution to ecology. Here we compared Daphnia from lakes with landlocked versus anadromous alewife for differences in rates of population growth in the presence and absence of predator cues over the course of a 39-day experiment. We predicted that predator-induced shifts in life history traits would facilitate faster rates of population growth. Contrary to our expectations, predator cue exposure did not alter rates of population growth. We instead found that Daphnia from lakes with landlocked alewife ultimately attained higher population densities (and exhibited faster population growth) when compared with Daphnia from lakes with anadromous alewife. Based on our previous work, these population level responses were unexpected, as Daphnia from lakes with landlocked alewife exhibit slower rates of somatic growth and delayed maturation. We discuss our results in lieu of the known differences in plasticity and how the population growth patterns may be influenced by resource limitation.     

Recent parallel divergence in body shape and diet source of alewife life history forms

Recent work suggests that juvenile alewives (Alosa pseudoharengus) share similar phenotypes among independently derived landlocked (freshwater resident) populations. Based on this observation, it is possible that the alewife life history forms represent a case of parallel adaptive divergence. To further evaluate this hypothesis, we describe patterns of body shape divergence between anadromous and landlocked alewife life history forms using geometric morphometrics. Our results suggest that body shape differs significantly between juveniles of the alewife forms: anadromous fish were more robust, with larger heads and deeper caudal peduncles, while landlocked fish from three independently isolated populations were more fusiform with thinner caudal peduncles and smaller heads. These differences matched population level dietary patterns, which suggest that anadromous fish consumed more littoral resources than landlocked fish. Finding consistent differences across populations of the same form supports the notion that landlocked alewives have diverged from their anadromous ancestors in a parallel manner, in response to pressures associated with being isolated in freshwater lakes. Comparing alewife phenotypes to expectations from the literature suggests that neither migration distance of the population, nor the relative availability of habitats in each lake, are likely drivers of the pattern we report. Instead, the pattern is consistent with the hypothesis that divergence between alewife forms results from the distinct effects of each form on its zooplankton prey.     

Independent evolutionary origins of landlocked alewife populations and rapid parallel evolution of phenotypic traits

Alewife, Alosa pseudoharengus, populations occur in two discrete life-history variants, an anadromous form and a landlocked (freshwater resident) form. Landlocked populations display a consistent pattern of life-history divergence from anadromous populations, including earlier age at maturity, smaller adult body size, and reduced fecundity. In Connecticut (USA), dams constructed on coastal streams separate anadromous spawning runs from lake-resident landlocked populations. Here, we used sequence data from the mtDNA control region and allele frequency data from five microsatellite loci to ask whether coastal Connecticut landlocked alewife populations are independently evolved from anadromous populations or whether they share a common freshwater ancestor. We then used microsatellite data to estimate the timing of the divergence between anadromous and landlocked populations. Finally, we examined anadromous and landlocked populations for divergence in foraging morphology and used divergence time estimates to calculate the rate of evolution for foraging traits. Our results indicate that landlocked populations have evolved multiple times independently. Tests of population divergence and estimates of gene flow show that landlocked populations are genetically isolated, whereas anadromous populations exchange genes. These results support a 'phylogenetic raceme' model of landlocked alewife divergence, with anadromous populations forming an ancestral core from which landlocked populations independently diverged. Divergence time estimates suggest that landlocked populations diverged from a common anadromous ancestor no longer than 5000 years ago and perhaps as recently as 300 years ago, depending on the microsatellite mutation rate assumed. Examination of foraging traits reveals landlocked populations to have significantly narrower gapes and smaller gill raker spacings than anadromous populations, suggesting that they are adapted to foraging on smaller prey items. Estimates of evolutionary rates (in haldanes) indicate rapid evolution of foraging traits, possibly in response to changes in available resources.     

A cascade of evolutionary change alters consumer-resource dynamics and ecosystem function

It is becoming increasingly clear that intraspecific evolutionary divergence influences the properties of populations, communities and ecosystems. The different ecological impacts of phenotypes and genotypes may alter selection on many species and promote a cascade of ecological and evolutionary change throughout the food web. Theory predicts that evolutionary interactions across trophic levels may contribute to hypothesized feedbacks between ecology and evolution. However, the importance of 'cascading evolutionary change' in a natural setting is unknown. In lakes in Connecticut, USA, variation in migratory behaviour and feeding morphology of a fish predator, the alewife (Alosa pseudoharengus), drives life-history evolution in a species of zooplankton prey (Daphnia ambigua). Here we evaluated the reciprocal impacts of Daphnia evolution on ecological processes in laboratory mesocosms. We show that life-history evolution in Daphnia facilitates divergence in rates of population growth, which in turn significantly alters consumer-resource dynamics and ecosystem function. These experimental results parallel trends observed in lakes. Such results argue that a cascade of evolutionary change, which has occurred over contemporary timescales, alters community and ecosystem processes.     

Interpopulation variation in a fish predator drives evolutionary divergence in prey in lakes

Ecological factors are known to cause evolutionary diversification. Recent work has shown that evolution in strongly interacting predator species has reciprocal impacts on ecosystems. These divergent impacts of predators may alter the selective landscape and cause the evolution of prey. Yet, this link between intraspecific variation and evolution is unexplored. We compared the life history of a species of zooplankton (Daphnia ambigua) from lakes in New England in which the dominant planktivorous predator, the alewife (Alosa pseudoharengus), differs in feeding traits and migratory behaviour. Anadromous alewife (seasonal migrants) exhibit larger gapes, gill-raker spacing and target larger prey than landlocked alewife (year-round freshwater resident). In 'anadromous' lakes, Daphnia are abundant in the spring but extirpated by alewife predation in summer. Daphnia are rare year-round in 'landlocked' lakes. We show that Daphnia from lakes with anadromous alewife grew faster, matured earlier but at the same size and produced more offspring than Daphnia from lakes with landlocked or no alewife across multiple temperature and resource treatments. Our results are inconsistent with a response to size-selective predation but are better explained as an adaptation to colder temperatures and shorter periods of development (countergradient variation) mediated by seasonal alewife predation.     

Phytoplankton composition modifies predator-driven life history evolution in Daphnia

Organisms experience competing selective pressures, which can obscure the mechanisms driving evolution. Daphnia ambigua is found in lakes where a predator, the alewife (Alosa pseudoharengus) either does (anadromous) or does not (landlocked) migrate between marine and freshwater. We previously reported an association between alewife variation and life history evolution in Daphnia. However, differences in alewife migration indirectly influence phytoplankton composition for Daphnia. In ‘anadromous lakes’, Daphnia are present in the spring and experience abundant high-quality green algae. Intense predation by young-of-the-year anadromous alewife quickly eliminates these Daphnia populations by early summer. Daphnia from ‘landlocked lakes’ and lakes without alewife (‘no alewife lakes’) are present during the spring and summer and are more likely to experience high concentrations of sub-optimal cyanobacteria during the summer. To explore links between predation, resources, and prey evolution, we reared third-generation laboratory-born Daphnia from all lake types on increasing cyanobacteria concentrations. We observed several significant ‘lake type × resource’ interactions whereby the differences among lake types depended upon cyanobacteria concentrations. Daphnia from anadromous lakes developed faster, were larger at maturation, produced more offspring, and had higher intrinsic rates of increase in the absence of cyanobacteria. Such trends disappeared or reversed as cyanobacteria concentration was increased because Daphnia from anadromous lakes were more strongly influenced by the presence of cyanobacteria. Our results argue that alewife migration and phytoplankton composition both play a role in Daphnia evolution.     

Mensurative approach to examine potential interactions between age-0 yellow perch (Perca flavescens) and bluegill (Lepomis macrochirus)

Bluegill (Lepomis macrochirus) and yellow perch (Perca flavescens) populations are often sympatric in the Great Plains region of the U.S.A. and portions of Canada; however, very little attention has been given to potential interactions between these species for available resources, especially during the early life stages. Relationships between age-0 bluegill and yellow perch growth and relative abundance were explored across multiple lakes and years within the Nebraska Sandhill region, USA. In addition, four habitat patch types (open water, Phragmites spp., Typha spp., Scirpus spp.) were sampled for age-0 bluegill and yellow perch, and food habits were examined for each species during August, September, and October of 2009 in one of these lakes. Age-0 yellow perch growth was negatively related to age-0 bluegill relative abundance across a spatiotemporal scale. Age-0 bluegill and yellow perch exhibited similar habitat use (moderate–high overlap), but generally consumed different important and dominant prey taxa (bluegill consumed both macroinvertebrates—56?% and zooplankton—44?%, while yellow perch consumed more zooplankton—66?%), which resulted in low overall diet overlap between species. Previous research indicates that age-0 yellow perch diet ontogeny often results in feeding predominately on macroinvertebrates and positively selecting them (and avoiding zooplankton prey) at sizes observed in our study. Therefore, yellow perch growth rates may be compromised by the presence of bluegill because of the need to consume less energetically profitable prey items such as zooplankton.     

The impact of intraspecific variation in a fish predator on the evolution of phenotypic plasticity and investment in sex in Daphnia ambigua

Theory predicts that the evolution of phenotypic plasticity depends upon cues that indicate environmental change. Predators typically induce plastic responses in prey. However, variation among populations of predators alters the frequency of predation and, possibly, the evolution of plasticity. We compared responses to predator cues in Daphnia ambigua from lakes where alewife (Alosa pseudoharengus) either do (anadromous) or do not (landlocked) migrate between marine and freshwater. In 'anadromous' lakes, Daphnia are abundant each spring but eliminated by alewives in summer, whereas Daphnia are constantly under the threat of predation in 'landlocked' lakes. Daphnia from 'anadromous' lakes grew faster, matured earlier and larger, produced more offspring and invested more in sex than Daphnia from landlocked lakes. We observed several significant lake type-by-predator treatment interactions. These interactions, whereby the differences between lakes were greater in predator-conditioned water, agree with theory and argue that Daphnia plasticity has been influenced by variation in alewives.     

The role of gill raker number variability in adaptive radiation of coregonid fish

Gill raker divergence is a general pattern in adaptive radiations of postglacial fish, but few studies have addressed the adaptive significance of this morphological trait in foraging and eco-evolutionary interactions among predator and prey. Here, a set of subarctic lakes along a diversifying gradient of coregonids was used as the natural setting to explore correlations between gill raker numbers and planktivory as well as the impact of coregonid radiation on zooplankton communities. Results from 19 populations covering most of the total gill raker number gradient of the genus Coregonus, confirm that the number of gill rakers has a central role in determining the foraging ability towards zooplankton prey. Both at the individual and population levels, gill raker number was correlated with pelagic niche use and the size of utilized zooplankton prey. Furthermore, the average body size and the abundance and diversity of the zooplankton community decreased with the increasing diversity of coregonids. We argue that zooplankton feeding leads to an eco-evolutionary feedback loop that may further shape the gill raker morphology since natural selection intensifies under resource competition for depleted prey communities. Eco-evolutionary interactions may thus have a central role creating and maintaining the divergence of coregonid morphs in postglacial lakes.     

Intraspecific variation in a predator drives cascading variation in primary producer community composition

Predation has important cascading impacts on primary producer biomass and community composition in many ecosystems. While most studies have focused on the consequences of interspecific or density differences in predators, it is recognized that phenotypic variation within species can have strong and cascading community and ecosystem consequences at lower trophic levels. In coastal New England lakes, both the presence and life history form of the zooplanktivorous fish alewife, Alosa pseudoharengus, have strong influence on the biomass, size structure and community composition of crustacean zooplankton communities. Here we test the hypothesis that alewife presence and life history will have cascading impacts on phytoplankton biomass and community composition in a mesocosm experiment that previously reported strong biomass and compositional differences of crustacean zooplankton communities among alewife treatments. We show that alewife life history led to small but statistically significant differences in phytoplankton community composition among treatments. This compositional difference was driven primarily by an increase in the density of two edible phytoplankton genera associated with lower zooplankton biomass in the anadromous alewife treatment. Our results show that intraspecific variation in a predator can have cascading effects on primary producer communities. However we did not observe significant differences in total algal biomass.     

Zooplankton responses to predation by larval bluegill: an enclosure experiment

SUMMARY 1. Larval fish are gape-limited predators that forage on prey of specific sizes, and thus may be expected to differentially affect members of a zooplankton community, possibly altering the size-structure or species composition.
2. I used an enclosure experiment to look at the effect of predation by larval bluegill on the dynamics of two zooplankton communities, one dominated by large-bodied individuals and the other by small-bodied individuals. Enclosures containing these zooplankton received a zero, low, medium, or high density of larval bluegill predators.
3. Increasing larval density had a negative effect on zooplankton abundance and abundance declined similarly in the large-bodied and small-bodied communities.
4. Zooplankton size-structure, as estimated by the length of the average zooplankton, increased and then decreased during the experiment, decreasing faster at higher larval fish densities. When zooplankton size-structure was estimated as the length of the average cladoceran, size-structure declined in the large-bodied but not in the small-bodied community and the greatest decline in size-structure was seen in the medium and high larval density treatments.
5. Ordination of each community using multidimensional scaling (MDS) indicated that the trajectory of change in species composition differed between the presence and absence of larval fish. In both communities, the degree of response by individual taxa depended on the density of bluegill larvae. This effect on zooplankton abundance, size-structure and community composition suggests that larval fish may make an important contribution to zooplankton dynamics in many lakes and ponds.     

Evolutionary history of Daphnia drives divergence in grazing selectivity and alters temporal community dynamics of producers

Consumers with different seasonal life histories encounter different communities of producers during specific seasonal phases. If consumers evolve to prefer the producers that they encounter, then consumers may reciprocally influence the temporal composition of producer communities. Here, we study the keystone consumer Daphnia ambigua, whose seasonal life history has diverged due to intraspecific predator divergence across lakes of New England. We ask whether grazing preferences of Daphnia have diverged also and test whether any grazing differences influence temporal composition patterns of producers. We reared clonal populations of Daphnia from natural populations representing the two diverged life history types for multiple generations. We conducted short‐term (24 hr) and long‐term (27 days) grazing experiments in equal polycultures consisting of three diatom and two green algae species, treated with no consumer, Daphnia from lakes with anadromous alewife, or from lakes with landlocked alewife. After 24 hr, life history and grazing preference divergence in Daphnia ambigua drove significant differences in producer composition. However, those differences disappeared at the end of the 27‐day experiment. Our results illustrate that, despite potentially more complex long‐term dynamics, a multitrophic cascade of evolutionary divergence from a predator can influence temporal community dynamics at the producer level.     

Indirect trophic interactions with an invasive species affect phenotypic divergence in a top consumer

While phenotypic responses to direct species interactions are well studied, we know little about the consequences of indirect interactions for phenotypic divergence. In this study we used lakes with and without the zebra mussel to investigate effects of indirect trophic interactions on phenotypic divergence between littoral and pelagic perch. We found a greater phenotypic divergence between littoral and pelagic individuals in lakes with zebra mussels and propose a mussel-mediated increase in pelagic and benthic resource availability as a major factor underlying this divergence. Lakes with zebra mussels contained higher densities of large plankton taxa and large invertebrates. We suggest that this augmented resource availability improved perch foraging opportunities in both the littoral and pelagic zones. Perch in both habitats could hence express a more specialized foraging morphology, leading to an increased divergence of perch forms in lakes with zebra mussels. As perch do not prey on mussels directly, we conclude that the increased divergence results from indirect interactions with the mussels. Our results hence suggest that species at lower food web levels can indirectly affect phenotypic divergence in species at the top of the food chain.     

Contemporary trait change in a classic ecological experiment: rapid decrease in alewife gill‐raker spacing following introduction to an inland lake

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Scaling-up anti-predator phenotypic responses of prey: impacts over multiple generations in a complex aquatic community

Non-consumptive effects (NCEs) of predators owing to induced changes in prey traits are predicted to influence the structure of ecological communities. However, evidence of the importance of NCEs is limited primarily to simple systems (e.g. two to four species) over relatively short periods (e.g. less than one generation). We examined the NCEs of a fish predator, arising from phenotypic plasticity in zooplankton prey traits, over multiple generations of a diverse zooplankton community. The presence of fish, caged to remove consumptive effects, strongly influenced zooplankton community structure, through both direct and indirect NCE pathways, altering the abundance of many taxa by magnitudes as large as 3 to 10-fold. Presence of fish affected different species of cladocerans and copepods both positively and negatively. A particularly striking result was the reversal of dominance in copepod taxa: presence of fish reduced the ratio of calanoids to cyclopoids from 6.3 to 0.43. Further, the NCE of fish had a strong negative trophic cascade to zooplankton resources (phytoplankton). To our knowledge, this is the first experiment to show that NCEs can influence the abundance of multiple prey species over time spans of multiple prey generations. Our findings demonstrate that adaptive phenotypic plasticity of individuals can scale-up to affect the structure of ecological communities.     

Selective predation on zooplankton by pelagic Arctic charr, Salvelinus alpinus, in six subarctic lakes

Selective predation by planktivore fish appears to be an important regulatory factor of zooplankton communities, potentially causing large changes in species composition and size distributions within populations. In this study, prey preferences and size-selective predation on zooplankton by Arctic charr were examined in six subarctic lakes with Arctic charr as the dominant pelagic fish species. Most of the lakes had a zooplankton community dominated by copepods (Cyclops scutifer and Eudiaptomus graciloides), but the pelagic charr evidently selected cladoceran species (Bythotrephes longimanus, Daphnia sp. and Bosmina sp.), likely because the copepods have a higher mobility and evasiveness than the cladocerans. Furthermore, a strong size selection was also revealed for both Bosmina sp. and Daphnia sp., as individual prey from Arctic charr stomachs were exclusively larger than individuals sampled in the environment. Additionally, visibility due to size, morphology and pigmentation (egg-carrying females) was also a major factor for the selection of zooplankton prey. In conclusion, Arctic charr was found to be highly selective on zooplankton both in respect to species composition and individual size of Bosmina sp. and Daphnia sp.     

The evolution of eye size in response to increased fish predation in Daphnia

Variation in eye size is ubiquitous across taxa. Increased eye size is correlated with improved vision and increased fitness via shifts in behavior. Tests of the drivers of eye size evolution have focused on macroevolutionary studies evaluating the importance of light availability. Predator‐induced mortality has recently been identified as a potential driver of eye size variation. Here, we tested the influence of increased predation by the fish predator, the alewife (Alosa pseudoharengus) on eye size evolution in waterfleas (Daphnia ambigua) from lakes in Connecticut. We quantified the relative eye size of Daphnia from lakes with and without alewife using wild‐caught and third‐generation laboratory reared specimens. This includes comparisons between lakes where alewife are present seasonally (anadromous) or permanently (landlocked). Wild‐caught specimens did not differ in eye size across all lakes. However, third‐generation lab reared Daphnia from lakes with alewife, irrespective of the form of alewife predation, exhibited significantly larger eyes than Daphnia from lakes without alewife. This genetically based increase in eye size may enhance the ability of Daphnia to detect predators. Alternatively, such shifts in eye size may be an indirect response to Daphnia aggregating at the bottom of lakes. To test these mechanisms, we collected Daphnia as a function of depth and found that eye size differed in Daphnia found at the surface versus the bottom of the water column between anadromous alewife and no alewife lakes. However, we found no evidence of Daphnia aggregating at the bottom of lakes. Such results indicate that the evolution of a larger eye may be explained by a connection between eyes and enhanced survival. We discuss the cause of the lack of concordance in eye size variation between our phenotypic and genetic specimens and the ultimate drivers of eye size.     

Role of epibenthic resource opportunities in the parallel evolution of lake whitefish species pairs (Coregonus sp.)

Parallel evolution of a dwarf and normal whitefish has been documented in six post-glacial lakes. Here, we relate the structure and seasonal variations of the epibenthic invertebrate communities to the extent of phenotypic differentiation in these species pairs. The highest phenotypic differentiation occurs in lakes characterized by less overlap in size distribution between limnetic and epibenthic prey which could represent enhanced ecological opportunities for trophic specialization and adaptive divergence. Differences in community assemblages and seasonal variation of biotic and abiotic conditions may also play a role. Accumulating evidence indicates that strong directional selection acting on dwarf whitefish may be more important than divergent selection acting on both sympatric forms in driving whitefish phenotypic divergence and ultimately, ecological speciation. Along with Landry et al. (2007), this study supports the general hypothesis that parallelism in divergence among sympatric dwarf and normal whitefish is associated with parallelism in limnological adaptive landscape.     

Preference for Cannibalism and Ontogenetic Constraints in Competitive Ability of Piscivorous Top Predators

Occurrence of cannibalism and inferior competitive ability of predators compared to their prey have been suggested to promote coexistence in size-structured intraguild predation (IGP) systems. The intrinsic size-structure of fish provides the necessary prerequisites to test whether the above mechanisms are general features of species interactions in fish communities where IGP is common. We first experimentally tested whether Arctic char (Salvelinus alpinus) were more efficient as a cannibal than as an interspecific predator on the prey fish ninespine stickleback (Pungitius pungitius) and whether ninespine stickleback were a more efficient competitor on the shared zooplankton prey than its predator, Arctic char. Secondly, we performed a literature survey to evaluate if piscivores in general are more efficient as cannibals than as interspecific predators and whether piscivores are inferior competitors on shared resources compared to their prey fish species. Both controlled pool experiments and outdoor pond experiments showed that char imposed a higher mortality on YOY char than on ninespine sticklebacks, suggesting that piscivorous char is a more efficient cannibal than interspecific predator. Estimates of size dependent attack rates on zooplankton further showed a consistently higher attack rate of ninespine sticklebacks compared to similar sized char on zooplankton, suggesting that ninespine stickleback is a more efficient competitor than char on zooplankton resources. The literature survey showed that piscivorous top consumers generally selected conspecifics over interspecific prey, and that prey species are competitively superior compared to juvenile piscivorous species in the zooplankton niche. We suggest that the observed selectivity for cannibal prey over interspecific prey and the competitive advantage of prey species over juvenile piscivores are common features in fish communities and that the observed selectivity for cannibalism over interspecific prey has the potential to mediate coexistence in size structured intraguild predation systems.