Phenotypic and transcriptional response of Daphnia pulicaria to the combined effects of temperature and predation.

Daphnia, an ecologically important zooplankton species in lakes, shows both genetic adaptation and phenotypic plasticity in response to temperature and fish predation, but little is known about the molecular basis of these responses and their potential interactions. We performed a factorial experiment exposing laboratory-propagated Daphnia pulicaria clones from two lakes in the Sierra Nevada mountains of California to normal or high temperature (15°C or 25°C) in the presence or absence of fish kairomones, then measured changes in life history and gene expression. Exposure to kairomones increased upper thermal tolerance limits for physiological activity in both clones. Cloned individuals matured at a younger age in response to higher temperature and kairomones, while size at maturity, fecundity and population intrinsic growth were only affected by temperature. At the molecular level, both clones expressed more genes differently in response to temperature than predation, but specific genes involved in metabolic, cellular, and genetic processes responded differently between the two clones. Although gene expression differed more between clones from different lakes than experimental treatments, similar phenotypic responses to predation risk and warming arose from these clone-specific patterns. Our results suggest that phenotypic plasticity responses to temperature and kairomones interact synergistically, with exposure to fish predators increasing the tolerance of Daphnia pulicaria to stressful temperatures, and that similar phenotypic responses to temperature and predator cues can be produced by divergent patterns of gene regulation.

An Empiricist's Guide to Using Ecological Theory.

AbstractA scientific understanding of the biological world arises when ideas about how nature works are formalized, tested, refined, and then tested again. Although the benefits of feedback between theoretical and empirical research are widely acknowledged by ecologists, this link is still not as strong as it could be in ecological research. This is in part because theory, particularly when expressed mathematically, can feel inaccessible to empiricists who may have little formal training in advanced math. To address this persistent barrier, we provide a general and accessible guide that covers the basic, step-by-step process of how to approach, understand, and use ecological theory in empirical work. We first give an overview of how and why mathematical theory is created, then outline four specific ways to use both mathematical and verbal theory to motivate empirical work, and finally present a practical tool kit for reading and understanding the mathematical aspects of ecological theory. We hope that empowering empiricists to embrace theory in their work will help move the field closer to a full integration of theoretical and empirical research.

Sierra Nevada mountain lake microbial communities are structured by temperature, resources and geographic location.

Warming, eutrophication (nutrient fertilization) and brownification (increased loading of allochthonous organic matter) are three global trends impacting lake ecosystems. However, the independent and synergistic effects of resource addition and warming on autotrophic and heterotrophic microorganisms are largely unknown. In this study, we investigate the independent and interactive effects of temperature, dissolved organic carbon (DOC, both allochthonous and autochthonous) and nitrogen (N) supply, in addition to the effect of spatial variables, on the composition, richness, and evenness of prokaryotic and eukaryotic microbial communities in lakes across elevation and N deposition gradients in the Sierra Nevada mountains of California, USA. We found that both prokaryotic and eukaryotic communities are structured by temperature, terrestrial (allochthonous) DOC and latitude. Prokaryotic communities are also influenced by total and aquatic (autochthonous) DOC, while eukaryotic communities are also structured by nitrate. Additionally, increasing N availability was associated with reduced richness of prokaryotic communities, and both lower richness and evenness of eukaryotes. We did not detect any synergistic or antagonistic effects as there were no interactions among temperature and resource variables. Together, our results suggest that (a) organic and inorganic resources, temperature, and geographic location (based on latitude and longitude) independently influence lake microbial communities; and (b) increasing N supply due to atmospheric N deposition may reduce richness of both prokaryotic and eukaryotic microbes, probably by reducing niche dimensionality. Our study provides insight into abiotic processes structuring microbial communities across environmental gradients and their potential roles in material and energy fluxes within and between ecosystems.

Predators drive community reorganization during experimental range shifts.

Increased global temperatures caused by climate change are causing species to shift their ranges and colonize new sites, creating novel assemblages that have historically not interacted. Species interactions play a central role in the response of ecosystems to climate change, but the role of trophic interactions in facilitating or preventing range expansions is largely unknown. The goal of our study was to understand how predators influence the ability of range-shifting prey to successfully establish in newly available habitat following climate warming. We hypothesized that fish predation facilitates the establishment of colonizing zooplankton populations, because fish preferentially consume larger species that would otherwise competitively exclude smaller-bodied colonists. We conducted a mesocosm experiment with zooplankton communities and their fish predators from lakes of the Sierra Nevada Mountains in California, USA. We tested the effect of fish predation on the establishment and persistence of a zooplankton community when introduced in the presence of higher- and lower-elevation communities at two experimental temperatures in field mesocosms. We found that predators reduce the abundance of larger-bodied residents from the alpine and facilitate the establishment of new lower-elevation species. In addition, fish predation and warming independently reduced the average body size of zooplankton by up to 30%. This reduction in body size offset the direct effect of warming-induced increases in population growth rates, leading to no net change in zooplankton biomass or trophic cascade strength. We found support for a shift to smaller species with climate change through two mechanisms: (a) the direct effects of warming on developmental rates and (b) size-selective predation that altered the identity of species' that could colonize new higher elevation habitat. Our results suggest that predators can amplify the rate of range shifts by consuming larger-bodied residents and facilitating the establishment of new species. However, the effects of climate warming were dampened by reducing the average body size of community members, leading to no net change in ecosystem function, despite higher growth rates. This work suggests that trophic interactions play a role in the reorganization of regional communities under climate warming.

Ecosystem effects of the world's largest invasive animal.

The keystone roles of mega-fauna in many terrestrial ecosystems have been lost to defaunation. Large predators and herbivores often play keystone roles in their native ranges, and some have established invasive populations in new biogeographic regions. However, few empirical examples are available to guide expectations about how mega-fauna affect ecosystems in novel environmental and evolutionary contexts. We examined the impacts on aquatic ecosystems of an emerging population of hippopotamus (Hippopotamus amphibus) that has been growing in Colombia over the last 25 yr. Hippos in Africa fertilize lakes and rivers by grazing on land and excreting wastes in the water. Stable isotopes indicate that terrestrial sources contribute more carbon in Colombian lakes containing hippo populations, and daily dissolved oxygen cycles suggest that their presence stimulates ecosystem metabolism. Phytoplankton communities were more dominated by cyanobacteria in lakes with hippos, and bacteria, zooplankton, and benthic invertebrate communities were similar regardless of hippo presence. Our results suggest that hippos recapitulate their role as ecosystem engineers in Colombia, importing terrestrial organic matter and nutrients with detectable impacts on ecosystem metabolism and community structure in the early stages of invasion. Ongoing range expansion may pose a threat to water resources.

Cryptic dispersal networks shape biodiversity in an invaded landscape.

Species interact with the physical world in complex ways, and life-history strategies could cause species to differ in how they experience the connectedness of the same landscape. As a consequence, dispersal limitation might be present but not captured by distance-based measures of connectivity. To test these ideas, we surveyed plant communities that live on discrete patches of serpentine habitat embedded within an invaded nonserpentine habitat matrix. Species in these communities differ in dispersal mode (gravity, animal, or wind); thus we used satellite imagery to quantify landscape features that might differentially influence connectivity for some dispersal- mode groups over others (surface streams, animal paths). Our data yielded two key insights: first, dispersal limitation appeared to be absent using a conventional distance-based measure of connectivity, but emerged after considering forms of landscape connectivity relevant to each dispersal mode. Second, the landscape variables that emerged as most important to each dispersal mode were generally consistent with our predictions based on species' putative dispersal vectors, but also included unexpected interactive effects. For example, the richness of animal-dispersed species was positively associated with animal connectivity when patches were close in space, but when patches were isolated, animals had a strong negative effect. This finding alludes to the reduced ability of animals to disperse seeds between suitable patches in invaded landscapes because of increased inter-patch distances. Real landscapes include complex spatial flows of energy and matter, which, as our work demonstrates, sets up ecological opportunity for organisms to differ in how they disperse in a common landscape.

Amino acid composition reveals functional diversity of zooplankton in tropical lakes related to geography, taxonomy and productivity.

Variation in resource use among species determines their potential for competition and co-existence, as well as their impact on ecosystem processes. Planktonic crustaceans consume a range of micro-organisms that vary among habitats and species, but these differences in resource consumption are difficult to characterize due to the small size of the organisms. Consumers acquire amino acids from their diet, and the composition of tissues reflects both the use of different resources and their assimilation in proteins. We examined the amino acid composition of common crustacean zooplankton from 14 tropical lakes in Colombia in three regions (the Amazon floodplain, the eastern range of the Andes, and the Caribbean coast). Amino acid composition varied significantly among taxonomic groups and the three regions. Functional richness in amino acid space was greatest in the Amazon, the most productive region, and tended to be positively related to lake trophic status, suggesting the niche breadth of the community could increase with ecosystem productivity. Functional evenness increased with lake trophic status, indicating that species were more regularly distributed within community-wide niche space in more productive lakes. These results show that zooplankton resource use in tropical lakes varies with both habitat and taxonomy, and that lake productivity may affect community functional diversity and the distribution of species within niche space.

Predators modify biogeographic constraints on species distributions in an insect metacommunity.

Theory describing the positive effects of patch size and connectivity on diversity in fragmented systems has stimulated a large body of empirical work, yet predicting when and how local species interactions mediate these responses remains challenging. We used insects that specialize on milkweed plants as a model metacommunity to investigate how local predation alters the effects of biogeographic constraints on species distributions. Species-specific dispersal ability and susceptibility to predation were used to predict when patch size and connectivity should shape species distributions, and when these should be modified by local predator densities. We surveyed specialist herbivores and their predators in milkweed patches in two matrix types, a forest and an old field. Predator-resistant species showed the predicted direct positive effects of patch size and connectivity on occupancy rates. For predator-susceptible species, predators consistently altered the impact of biogeographic constraints, rather than acting independently. Finally, differences between matrix types in species' responses and overall occupancy rates indicate a potential role of the inter-patch environment in mediating the joint effects of predators and spatial drivers. Together, these results highlight the importance of local top-down pressure in mediating classic biogeographic relationships, and demonstrate how species-specific responses to local and regional constraints can be used to predict these effects.

Changing climate cues differentially alter zooplankton dormancy dynamics across latitudes.

In seasonal climates, dormancy is a common strategy that structures biodiversity and is necessary for the persistence of many species. Climate change will likely alter dormancy dynamics in zooplankton, the basis of aquatic food webs, by altering two important hatching cues: mean temperatures during the ice-free season, and mean day length when lakes become ice free. Theory suggests that these changes could alter diversity, hatchling abundances and phenology within lakes, and that these responses may diverge across latitudes due to differences in optimal hatching cues and strategies. To examine the role of temperature and day length on hatching dynamics, we collected sediment from 25 lakes across a 1800 km latitudinal gradient and exposed sediment samples to a factorial combination of two photoperiods (12 and 16 h) and two temperatures (8 and 12 °C) representative of historical southern (short photoperiod, warm) and northern (long photoperiod, cool) lake conditions. We tested whether sensitivity to these hatching cues varies by latitudinal origin and differs among taxa. Higher temperatures advanced phenology for all taxa, and these advances were greatest for cladocerans followed by copepods and rotifers. Although phenology differed among taxa, the effect of temperature did not vary with latitude. The latitudinal origin of the egg bank influenced egg abundance and hatchling abundance and diversity, with these latter effects varying with taxa, temperature and photoperiod. Copepod hatchling abundances peaked at mid-latitudes in the high temperature and long photoperiod treatments, whereas hatchling abundances of other zooplankton were greatest at low latitudes and high temperature. The overall diversity of crustacean zooplankton (copepods and cladocerans) also reflected distinct responses of each taxa to our treatments, with the greatest diversity occurring at mid-latitudes (~56 °N) in the shorter photoperiod treatment. Our results demonstrate that hatching cues differ for broad taxonomic groups that vary in developmental and life-history strategies. These differences are predicted to drive latitude-specific shifts in zooplankton emergence with climate change and could alter the base of aquatic food webs.

Consumer-based limitations drive oak recruitment failure.

A number of North American oaks are experiencing recruitment failure, with explanatory hypotheses including a range of consumer- or resource-based limitations. Using a factorial experiment with transplanted seedlings, we demonstrate how direct and indirect consumer effects prevent recruitment by Quercus garryana, a keystone savanna species of northwestern North America. Foremost, intense herbivory by mostly exotic small mammals severely damaged or killed 100% of unprotected seedlings during winter. Many damaged seedlings survived but were 64% smaller in size and produced 75% fewer leaves. Herbivory by deer had no detectable impact despite being long hypothesized as a major contributor to oak decline. Indirectly, herbivory altered the outcome of moisture limitation and competition. Without small mammals, summer drought and a dense exotic grass cover associated with fire suppression significantly reduced growth but caused little mortality. With small mammals, both significantly increased mortality of herbivore-damaged seedlings. Herbivore damage also increased the likelihood of severe insect attack, possibly due to reduced investment in foliar defense by recovering seedlings. These results show that no single factor necessarily prevents seedling establishment by oaks, but that the combination of herbivory, undisturbed exotic grass swards, and summer drought creates an almost insurmountable barrier for recruitment.