Does Intraspecific Size Variation in a Predator Affect Its Diet Diversity and Top-Down Control of Prey?

It has long been known that intraspecific variation impacts evolutionary processes, but only recently have its potential ecological effects received much attention. Theoretical models predict that genetic or phenotypic variance within species can alter interspecific interactions, and experiments have shown that genotypic diversity in clonal species can impact a wide range of ecological processes. To extend these studies to quantitative trait variation within populations, we experimentally manipulated the variance in body size of threespine stickleback in enclosures in a natural lake environment. We found that body size of stickleback in the lake is correlated with prey size and (to a lesser extent) composition, and that stickleback can exert top-down control on their benthic prey in enclosures. However, a six-fold contrast in body size variance had no effect on the degree of diet variation among individuals, or on the abundance or composition of benthic or pelagic prey. Interestingly, post-hoc analyses revealed suggestive correlations between the degree of diet variation and the strength of top-down control by stickleback. Our negative results indicate that, unless the correlation between morphology and diet is very strong, ecological variation among individuals may be largely decoupled from morphological variance. Consequently we should be cautious in our interpretation both of theoretical models that assume perfect correlations between morphology and diet, and of empirical studies that use morphological variation as a proxy for resource use diversity.     

Environmental fluctuations restrict eco-evolutionary dynamics in predator–prey system

Environmental fluctuations, species interactions and rapid evolution are all predicted to affect community structure and their temporal dynamics. Although the effects of the abiotic environment and prey evolution on ecological community dynamics have been studied separately, these factors can also have interactive effects. Here we used bacteria–ciliate microcosm experiments to test for eco-evolutionary dynamics in fluctuating environments. Specifically, we followed population dynamics and a prey defence trait over time when populations were exposed to regular changes of bottom-up or top-down stressors, or combinations of these. We found that the rate of evolution of a defence trait was significantly lower in fluctuating compared with stable environments, and that the defence trait evolved to lower levels when two environmental stressors changed recurrently. The latter suggests that top-down and bottom-up changes can have additive effects constraining evolutionary response within populations. The differences in evolutionary trajectories are explained by fluctuations in population sizes of the prey and the predator, which continuously alter the supply of mutations in the prey and strength of selection through predation. Thus, it may be necessary to adopt an eco-evolutionary perspective on studies concerning the evolution of traits mediating species interactions.     

Sex ratio variation shapes the ecological effects of a globally introduced freshwater fish

Sex ratio and sexual dimorphism have long been of interest in population and evolutionary ecology, but consequences for communities and ecosystems remain untested. Sex ratio could influence ecological conditions whenever sexual dimorphism is associated with ecological dimorphism in species with strong ecological interactions. We tested for ecological implications of sex ratio variation in the sexually dimorphic western mosquitofish, Gambusia affinis. This species causes strong pelagic trophic cascades and exhibits substantial variation in adult sex ratios. We found that female-biased populations induced stronger pelagic trophic cascades compared with male-biased populations, causing larger changes to key community and ecosystem responses, including zooplankton abundance, phytoplankton abundance, productivity, pH and temperature. The magnitude of such effects indicates that sex ratio is important for mediating the ecological role of mosquitofish. Because both sex ratio variation and sexual dimorphism are common features of natural populations, our findings should encourage broader consideration of the ecological significance of sex ratio variation in nature, including the relative contributions of various sexually dimorphic traits to these effects.     

Ecological and Evolutionary Effects of Stickleback on Community Structure

Species’ ecology and evolution can have strong effects on communities. Both may change concurrently when species colonize a new ecosystem. We know little, however, about the combined effects of ecological and evolutionary change on community structure. We simultaneously examined the effects of top-predator ecology and evolution on freshwater community parameters using recently evolved generalist and specialist ecotypes of three-spine stickleback (Gasterosteus aculeatus). We used a mesocosm experiment to directly examine the effects of ecological (fish presence and density) and evolutionary (phenotypic diversity and specialization) factors on community structure at lower trophic levels. We evaluated zooplankton biomass and composition, periphyton and phytoplankton chlorophyll-a concentration, and net primary production among treatments containing different densities and diversities of stickleback. Our results showed that both ecological and evolutionary differences in the top-predator affect different aspects of community structure and composition. Community structure, specifically the abundance of organisms at each trophic level, was affected by stickleback presence and density, whereas composition of zooplankton was influenced by stickleback diversity and specialization. Primary productivity, in terms of chlorophyll-a concentration and net primary production was affected by ecological but not evolutionary factors. Our results stress the importance of concurrently evaluating both changes in density and phenotypic diversity on the structure and composition of communities.     

Prey productivity effects on the impact of predators of the mussel, Mytilus californianus (Conrad)

The relationship of increasing prey productivity, a measure incorporating prey settlement and body growth, to changes in the relative impact of two predator groups, birds and the sea star, Pisaster ochraceus (Brandt) on a competitively dominant mussel, Mytilus californianus were examined. The purpose of this experiment was twofold, 1) to determine if the separate effects of each predator group on prey abundance increased as prey productivity increased and 2) to determine if the relative impacts of the two predator groups diverged as prey productivity increased. In this experiment, the separate impact of each predator group increased with increasing prey productivity. However, the relative impact of each predator group did not diverge with increasing prey productivity. Unlike previous studies that suggested with increasing prey productivity the relative effect of two predator groups should diverge, this experiment suggested that communities can have more redundant predator groups than originally thought. The results of an analysis using a proportional hazards model suggested that despite increasing prey productivity, birds and the sea star were equal in their ability to curb population increases by M. californianus. These results highlight the need to carefully consider what type of species to species comparisons to make when attempting to discern the relative roles of different predator groups in a community.     

Predator cannibalism can shift prey community composition toward dominance by small prey species

Cannibalism among predators is a key intraspecific interaction affecting their density and foraging behavior, eventually modifying the strength of predation on heterospecific prey. Interestingly, previous studies showed that cannibalism among predators can increase or reduce predation on heterospecific prey; however, we know less about the factors that lead to these outcomes. Using a simple pond community consisting of Hynobius retardatus salamander larvae and their associated prey, I report empirical evidence that cannibalism among predators can increase predation on large heterospecific prey but reduce that on small heterospecific prey. In a field‐enclosure experiment in which I manipulated the occurrence of salamander cannibalism, I found that salamander cannibalism increased predation on frog tadpoles but reduced that on aquatic insects simultaneously. The contrasting effects are most likely to be explained by prey body size. In the study system, frog tadpoles were too large for non‐cannibal salamanders to consume, while aquatic insects were within the non‐cannibals’ consumable prey size range. However, when cannibalism occurred, a few individuals that succeeded in cannibalizing reached large enough size to consume frog tadpoles. Consequently, although cannibalism among salamanders reduced their density, salamander cannibalism increased predation on large prey frog tadpoles. Meanwhile, salamander cannibalism reduced predation on small prey aquatic insects probably because of a density reduction of non‐cannibals primarily consuming aquatic insects. Body size is often correlated with various ecological traits, for instance, diet width, consumption, and excretion rates, and is thus considered a good indicator of species’ effects on ecosystem function. All this considered, cannibalism among predators could eventually affect ecosystem function by shifting the size composition of the prey community.     

Linking killer whale survival and prey abundance: food limitation in the oceans' apex predator?

Killer whales (Orcinus orca) are large predators that occupy the top trophic position in the world''s oceans and as such may have important roles in marine ecosystem dynamics. Although the possible top-down effects of killer whale predation on populations of their prey have received much recent attention, little is known of how the abundance of these predators may be limited by bottom-up processes. Here we show, using 25 years of demographic data from two populations of fish-eating killer whales in the northeastern Pacific Ocean, that population trends are driven largely by changes in survival, and that survival rates are strongly correlated with the availability of their principal prey species, Chinook salmon (Oncorhynchus tshawytscha). Our results suggest that, although these killer whales may consume a variety of fish species, they are highly specialized and dependent on this single salmonid species to an extent that it is a limiting factor in their population dynamics. Other ecologically specialized killer whale populations may be similarly constrained to a narrow range of prey species by culturally inherited foraging strategies, and thus are limited in their ability to adapt rapidly to changing prey availability.     

The community and ecosystem consequences of intraspecific diversity: a meta‐analysis

Understanding the relationships between biodiversity and ecosystem functioning has major implications. Biodiversity–ecosystem functioning relationships are generally investigated at the interspecific level, although intraspecific diversity (i.e. within‐species diversity) is increasingly perceived as an important ecological facet of biodiversity. Here, we provide a quantitative and integrative synthesis testing, across diverse plant and animal species, whether intraspecific diversity is a major driver of community dynamics and ecosystem functioning. We specifically tested (i) whether the number of genotypes/phenotypes (i.e. intraspecific richness) or the specific identity of genotypes/phenotypes (i.e. intraspecific variation) in populations modulate the structure of communities and the functioning of ecosystems, (ii) whether the ecological effects of intraspecific richness and variation are strong in magnitude, and (iii) whether these effects vary among taxonomic groups and ecological responses. We found a non‐linear relationship between intraspecific richness and community and ecosystem dynamics that follows a saturating curve shape, as observed for biodiversity–function relationships measured at the interspecific level. Importantly, intraspecific richness modulated ecological dynamics with a magnitude that was equal to that previously reported for interspecific richness. Our results further confirm, based on a database containing more than 50 species, that intraspecific variation also has substantial effects on ecological dynamics. We demonstrated that the effects of intraspecific variation are twice as high as expected by chance, and that they might have been underestimated previously. Finally, we found that the ecological effects of intraspecific variation are not homogeneous and are actually stronger when intraspecific variation is manipulated in primary producers than in consumer species, and when they are measured at the ecosystem rather than at the community level. Overall, we demonstrated that the two facets of intraspecific diversity (richness and variation) can both strongly affect community and ecosystem dynamics, which reveals the pivotal role of within‐species biodiversity for understanding ecological dynamics.     

Invasion strategies in clonal aquatic plants: are phenotypic differences caused by phenotypic plasticity or local adaptation?

Background and Aims

The successful spread of invasive plants in new environments is often linked to multiple introductions and a diverse gene pool that facilitates local adaptation to variable environmental conditions. For clonal plants, however, phenotypic plasticity may be equally important. Here the primary adaptive strategy in three non-native, clonally reproducing macrophytes (Egeria densa, Elodea canadensis and Lagarosiphon major) in New Zealand freshwaters were examined and an attempt was made to link observed differences in plant morphology to local variation in habitat conditions.

Methods

Field populations with a large phenotypic variety were sampled in a range of lakes and streams with different chemical and physical properties. The phenotypic plasticity of the species before and after cultivation was studied in a common garden growth experiment, and the genetic diversity of these same populations was also quantified.

Key Results

For all three species, greater variation in plant characteristics was found before they were grown in standardized conditions. Moreover, field populations displayed remarkably little genetic variation and there was little interaction between habitat conditions and plant morphological characteristics.

Conclusions

The results indicate that at the current stage of spread into New Zealand, the primary adaptive strategy of these three invasive macrophytes is phenotypic plasticity. However, while limited, the possibility that genetic diversity between populations may facilitate ecotypic differentiation in the future cannot be excluded. These results thus indicate that invasive clonal aquatic plants adapt to new introduced areas by phenotypic plasticity. Inorganic carbon, nitrogen and phosphorous were important in controlling plant size of E. canadensis and L. major, but no other relationships between plant characteristics and habitat conditions were apparent. This implies that within-species differences in plant size can be explained by local nutrient conditions. All together this strongly suggests that invasive clonal aquatic plants adapt to a wide range of habitats in introduced areas by phenotypic plasticity rather than local adaptation.     

Highly local environmental variability promotes intrapopulation divergence of quantitative traits: an example from tropical rain forest trees

Background and Aims

In habitat mosaics, plant populations face environmental heterogeneity over short geographical distances. Such steep environmental gradients can induce ecological divergence. Lowland rainforests of the Guiana Shield are characterized by sharp, short-distance environmental variations related to topography and soil characteristics (from waterlogged bottomlands on hydromorphic soils to well-drained terra firme on ferralitic soils). Continuous plant populations distributed along such gradients are an interesting system to study intrapopulation divergence at highly local scales. This study tested (1) whether conspecific populations growing in different habitats diverge at functional traits, and (2) whether they diverge in the same way as congeneric species having different habitat preferences.

Methods

Phenotypic differentiation was studied within continuous populations occupying different habitats for two congeneric, sympatric, and ecologically divergent tree species (Eperua falcata and E. grandiflora, Fabaceae). Over 3000 seeds collected from three habitats were germinated and grown in a common garden experiment, and 23 morphological, biomass, resource allocation and physiological traits were measured.

Key Results

In both species, seedling populations native of different habitats displayed phenotypic divergence for several traits (including seedling growth, biomass allocation, leaf chemistry, photosynthesis and carbon isotope composition). This may occur through heritable genetic variation or other maternally inherited effects. For a sub-set of traits, the intraspecific divergence associated with environmental variation coincided with interspecific divergence.

Conclusions

The results indicate that mother trees from different habitats transmit divergent trait values to their progeny, and suggest that local environmental variation selects for different trait optima even at a very local spatial scale. Traits for which differentiation within species follows the same pattern as differentiation between species indicate that the same ecological processes underlie intra- and interspecific variation.     

Testing a ‘genes‐to‐ecosystems’ approach to understanding aquatic–terrestrial linkages

A ‘genes‐to‐ecosystems’ approach has been proposed as a novel avenue for integrating the consequences of intraspecific genetic variation with the underlying genetic architecture of a species to shed light on the relationships among hierarchies of ecological organization (genes → individuals → communities → ecosystems). However, attempts to identify genes with major effect on the structure of communities and/or ecosystem processes have been limited and a comprehensive test of this approach has yet to emerge. Here, we present an interdisciplinary field study that integrated a common garden containing different genotypes of a dominant, riparian tree, Populus trichocarpa, and aquatic mesocosms to determine how intraspecific variation in leaf litter alters both terrestrial and aquatic communities and ecosystem functioning. Moreover, we incorporate data from extensive trait screening and genome‐wide association studies estimating the heritability and genes associated with litter characteristics. We found that tree genotypes varied considerably in the quality and production of leaf litter, which contributed to variation in phytoplankton abundances, as well as nutrient dynamics and light availability in aquatic mesocosms. These ‘after‐life’ effects of litter from different genotypes were comparable to the responses of terrestrial communities associated with the living foliage. We found that multiple litter traits corresponding with aquatic community and ecosystem responses differed in their heritability. Moreover, the underlying genetic architecture of these traits was complex, and many genes contributed only a small proportion to phenotypic variation. Our results provide further evidence that genetic variation is a key component of aquatic–terrestrial linkages, but challenge the ability to predict community or ecosystem responses based on the actions of one or a few genes.     

The effect of top‐predator presence and phenotype on aquatic microbial communities

The presence of predators can impact a variety of organisms within the ecosystem, including microorganisms. Because the effects of fish predators and their phenotypic differences on microbial communities have not received much attention, we tested how the presence/absence, genotype, and plasticity of the predatory three‐spine stickleback (Gasterosteus aculeatus) influence aquatic microbes in outdoor mesocosms. We reared lake and stream stickleback genotypes on contrasting food resources to adulthood, and then added them to aquatic mesocosm ecosystems to assess their impact on the planktonic bacterial community. We also investigated whether the effects of fish persisted following the removal of adults, and the subsequent addition of a homogenous juvenile fish population. The presence of adult stickleback increased the number of bacterial OTUs and altered the size structure of the microbial community, whereas their phenotype affected bacterial community composition. Some of these effects were detectable after adult fish were removed from the mesocosms, and after juvenile fish were placed in the tanks, most of these effects disappeared. Our results suggest that fish can have strong short‐term effects on microbial communities that are partially mediated by phenotypic variation of fish.     

Evidence for carry-over effects of predator exposure on pathogen transmission potential

Accumulating evidence indicates that species interactions such as competition and predation can indirectly alter interactions with other community members, including parasites. For example, presence of predators can induce behavioural defences in the prey, resulting in a change in susceptibility to parasites. Such predator-induced phenotypic changes may be especially pervasive in prey with discrete larval and adult stages, for which exposure to predators during larval development can have strong carry-over effects on adult phenotypes. To the best of our knowledge, no study to date has examined possible carry-over effects of predator exposure on pathogen transmission. We addressed this question using a natural food web consisting of the human malaria parasite Plasmodium falciparum, the mosquito vector Anopheles coluzzii and a backswimmer, an aquatic predator of mosquito larvae. Although predator exposure did not significantly alter mosquito susceptibility to P. falciparum, it incurred strong fitness costs on other key mosquito life-history traits, including larval development, adult size, fecundity and longevity. Using an epidemiological model, we show that larval predator exposure should overall significantly decrease malaria transmission. These results highlight the importance of taking into account the effect of environmental stressors on disease ecology and epidemiology.     

Prey bacteria shape the community structure of their predators

Although predator–prey interactions among higher organisms have been studied extensively, only few examples are known for microbes other than protists and viruses. Among the bacteria, the most studied obligate predators are the Bdellovibrio and like organisms (BALOs) that prey on many other bacteria. In the macroscopical world, both predator and prey influence the population size of the other''s community, and may have a role in selection. However, selective pressures among prey and predatory bacteria have been rarely investigated. In this study, Bacteriovorax, a predator within the group of BALOs, in environmental waters were fed two prey bacteria, Vibrio vulnificus and Vibrio parahaemolyticus. The two prey species yielded distinct Bacteriovorax populations, evidence that selective pressures shaped the predator community and diversity. The results of laboratory experiments confirmed the differential predation of Bacteriovorax phylotypes on the two bacteria species. Not only did Bacteriovorax Cluster IX exhibit the versatility to be the exclusive efficient predator on Vibrio vulnificus, thereby, behaving as a specialist, but was also able to prey with similar efficiency on Vibrio parahaemolyticus, indicative of a generalist. Therefore, we proposed a designation of versatilist for this predator. This initiative should provide a basis for further efforts to characterize the predatory patterns of bacterial predators. The results of this study have revealed impacts of the prey on Bacteriovorax predation and in structuring the predator community, and advanced understanding of predation behavior in the microbial world.     

Intraspecific shape variation in horseshoe crabs: The importance of sexual and natural selection for local adaptation

A morphometric analysis of the body shape of three species of horseshoe crabs was undertaken in order to infer the importance of natural and sexual selection. It was expected that natural selection would be most intense, leading to highest regional differentiation, in the American species Limulus polyphemus, which has the largest climatic differences between different populations. Local adaptation driven by sexual selection was expected in males but not females because horseshoe crab mating behaviour leads to competition between males, but not between females. Three hundred fifty-nine horseshoe crabs from nine populations, representing three species, were analyzed using a digitizer to position sixty morphometric landmarks in a three-dimensional space. Discriminant analysis revealed strong regional structuring within a species, which suggests strong philopatry, and showed the existence of geographically-based intraspecific variation. An admixture analysis showed regional intraspecific differentiation for males and females of L. polyphemus and males of the Asian horseshoe crab Carcinoscorpius rotundicauda, but not for females of C. rotundicauda and another Asian horseshoe crab, Tachypleus gigas. Differences in shape variation between sexes were tested with F-tests, which showed lower intrapopulation morphometric variation in males than females. These results indicate a lower degree of local adaptation on body shape in C. rotundicauda and T. gigas than in L. polyphemus and a lower degree of local adaptation in females than in males.     

Genetic architecture of a feeding adaptation: garter snake (Thamnophis) resistance to tetrodotoxin bearing prey

Detailing the genetic basis of adaptive variation in natural populations is a first step towards understanding the process of adaptive evolution, yet few ecologically relevant traits have been characterized at the genetic level in wild populations. Traits that mediate coevolutionary interactions between species are ideal for studying adaptation because of the intensity of selection and the well-characterized ecological context. We have previously described the ecological context, evolutionary history and partial genetic basis of tetrodotoxin (TTX) resistance in garter snakes (Thamnophis). Derived mutations in a voltage-gated sodium channel gene (Na_v1.4) in three garter snake species are associated with resistance to TTX, the lethal neurotoxin found in their newt prey (Taricha). Here we evaluate the contribution of Na_v1.4 alleles to TTX resistance in two of those species from central coastal California. We measured the phenotypes (TTX resistance) and genotypes (Na_v1.4 and microsatellites) in a local sample of Thamnophis atratus and Thamnophis sirtalis. Allelic variation in Na_v1.4 explains 23 per cent of the variation in TTX resistance in T. atratus while variation in a haphazard sample of the genome (neutral microsatellite markers) shows no association with the phenotype. Similarly, allelic variation in Na_v1.4 correlates almost perfectly with TTX resistance in T. sirtalis, but neutral variation does not. These strong correlations suggest that Na_v1.4 is a major effect locus. The simple genetic architecture of TTX resistance in garter snakes may significantly impact the dynamics of phenotypic coevolution. Fixation of a few alleles of major effect in some garter snake populations may have led to the evolution of extreme phenotypes and an ‘escape’ from the arms race with newts.     

Intraspecific variation in tolerance of warming in fishes

Intraspecific variation in key traits such as tolerance of warming can have profound effects on ecological and evolutionary processes, notably responses to climate change. The empirical evidence for three primary elements of intraspecific variation in tolerance of warming in fishes is reviewed. The first is purely mechanistic that tolerance varies across life stages and as fishes become mature. The limited evidence indicates strongly that this is the case, possibly because of universal physiological principles. The second is intraspecific variation that is because of phenotypic plasticity, also a mechanistic phenomenon that buffers individuals’ sensitivity to negative impacts of global warming in their lifetime, or to some extent through epigenetic effects over successive generations. Although the evidence for plasticity in tolerance to warming is extensive, more work is required to understand underlying mechanisms and to reveal whether there are general patterns. The third element is intraspecific variation based on heritable genetic differences in tolerance, which underlies local adaptation and may define long-term adaptability of a species in the face of ongoing global change. There is clear evidence of local adaptation and some evidence of heritability of tolerance to warming, but the knowledge base is limited with detailed information for only a few model or emblematic species. There is also strong evidence of structured variation in tolerance of warming within species, which may have ecological and evolutionary significance irrespective of whether it reflects plasticity or adaptation. Although the overwhelming consensus is that having broader intraspecific variation in tolerance should reduce species vulnerability to impacts of global warming, there are no sufficient data on fishes to provide insights into particular mechanisms by which this may occur.     

Effects of an invasive plant transcend ecosystem boundaries through a dragonfly-mediated trophic pathway

Trophic interactions can strongly influence the structure and function of terrestrial and aquatic communities through top-down and bottom-up processes. Species with life stages in both terrestrial and aquatic systems may be particularly likely to link the effects of trophic interactions across ecosystem boundaries. Using experimental wetlands planted with purple loosestrife (Lythrum salicaria), we tested the degree to which the bottom-up effects of floral density of this invasive plant could trigger a chain of interactions, changing the behavior of terrestrial flying insect prey and predators and ultimately cascading through top-down interactions to alter lower trophic levels in the aquatic community. The results of our experiment support the linkage of terrestrial and aquatic food webs through this hypothesized pathway, with high loosestrife floral density treatments attracting high levels of visiting insect pollinators and predatory adult dragonflies. High floral densities were also associated with increased adult dragonfly oviposition and subsequently high larval dragonfly abundance in the aquatic community. Finally, high-flower treatments were coupled with changes in zooplankton species richness and shifts in the composition of zooplankton communities. Through changes in animal behavior and trophic interactions in terrestrial and aquatic systems, this work illustrates the broad and potentially cryptic effects of invasive species, and provides additional compelling motivation for ecologists to conduct investigations that cross traditional ecosystem boundaries.     

Proximate stimuli: An overlooked driving force for risk-induced trait responses affecting interactions in aquatic ecosystems

Inducible responses in prey to predation risk can influence species interaction strength, with significant ecological consequences. Much of the past research on interactions in aquatic ecosystems has focused on remote stimuli (e.g., diffusible chemicals emitted from predators and injured conspecifics, which easily propagate through environmental water), as cues triggering trait responses in prey, and has overlooked the importance of proximate stimuli (e.g., physical disturbance and less-diffusible chemicals), which occur in attack or direct contact to prey by predators. Proximate stimuli from predators as well as remote stimuli may induce significant responses in prey functional traits such as behavior, morphology, and life history and, therefore, act as an important mechanism of top-down effects in aquatic ecosystems. In this opinion paper, we argue that studying the effects of proximate stimuli is essential to better understanding of individual adaptation to predation risk in nature and ecological consequences of predator–prey interactions. Here, we propose research directions to examine the role of proximate stimuli for phenotypic plasticity and interaction systems.