skip to main content


Title: Eutrophication‐driven eco‐evolutionary dynamics indicated by differences in stoichiometric traits among populations of Daphnia pulicaria
Abstract

Microevolution can have consequences at higher levels of ecological organization. Although divergence among populations can be rapid and driven by anthropogenic changes to the environment, the ecological relevance of evolution induced by human activities remains poorly understood.

A frequent way in which human activities drive microevolution is the increase in supply of nutrients such as phosphorus (P) that are required for fitness‐relevant traits such as growth and reproduction. Because higher P concentrations decrease P‐use efficiency and feeding rate in heterotrophic consumers such asDaphnia, we hypothesized that such adjustments should alter consumer–resource dynamics.

We examined how cultural eutrophication in temperate lakes causes trait variation in the grazerDaphnia pulicaria. We tested for variation inDaphniatraits and genetic variation in the metabolic enzyme phosphoglucose isomerase (Pgi) which are each known to respond to eutrophication. We then examined the impact of this variation on consumer–resource dynamics using a combination of experiments and a multi‐lake survey.

We found thatDaphniafrom hypereutrophic lakes responded to experimental hypereutrophic conditions with increased growth rates and fecundity when raised on P‐fertilized seston, but had reduced performance on P‐poor seston relative to eutrophic sourceDaphnia. These results suggest thatDaphniamay face a trade‐off in performance at low versus excess P that may be mediated in part by genetic variation at thePgilocus.

The variation observed in laboratory growth experiments scaled up toDaphniapopulations in both mesocosm experiments and among lakes. In both the mesocosm experiment and in the lake survey,Daphniafrom hypereutrophic source lakes reached high biomass while phytoplankton biomass also remained high.

Given the prevalence and rapid eutrophication of freshwater ecosystems worldwide, these results indicate that considering the potential effects of evolutionary change in ecosystem models could be useful in forecasting the effects of anthropogenic environmental change on pivotal ecosystem services.

 
more » « less
NSF-PAR ID:
10445266
Author(s) / Creator(s):
 ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Freshwater Biology
Volume:
67
Issue:
2
ISSN:
0046-5070
Page Range / eLocation ID:
p. 353-364
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Laboratory studies have revealed thatDaphniaspecies can evolve to tolerate toxic cyanobacteria in the diet. Specifically,Daphniafrom eutrophic lakes where cyanobacteria are common tend to have higher growth rates and survival when fed toxic cyanobacteria than populations from oligotrophic environments with low abundance of cyanobacteria.

    We conducted an in‐lake mesocosm (i.e. limnocorral) experiment during the autumn of 2009 to assess the effects of nutrient enrichment on clonal evolution inDaphnia pulicaria. As nutrient enrichment often favours grazing‐resistant cyanobacteria, we hypothesised that fertilisation would influence the genotypic composition ofD. pulicariathat vary in tolerance to cyanobacteria. Mesocosms were fertilised to manipulate phytoplankton and cyanobacterial abundance and concentrations of a cyanobacterial toxin (microcystin). Thus, half of the mesocosms were high‐nutrient and half were low‐nutrient. We then stocked half of the mesocosms with a mixture of six genetically‐distinctD. pulicariagenotypes (three genotypes from oligotrophic lakes and three from eutrophic lakes) leaving half of the mesocosmsDaphnia‐free to assess grazing effects, using a fully factorial design.

    When compared to the low nutrient treatment, high nutrient mesocosms had nearly five‐fold higher chlorophyllaconcentrations, eight‐fold higher cyanobacterial dry biomass, and three‐fold higher microcystin levels at the start of the experiment. In contrast, low nutrient mesocosms had phytoplankton concentrations typical of mesotrophic lakes.

    Fertilisation strongly affectedDaphniagenetic diversity in the mesocosms. FinalDaphniagenotype diversity in the mesocosms with low‐cyanobacteria (richness = 5.83, Shannon–Weiner index = 1.55, evenness = 0.88) was similar to the initial stocked diversity (richness = 5.50, Shannon–Weiner index = 1.48, evenness = 0.87). In contrast, final diversity in fertilised mesocosms with high cyanobacteria was greatly reduced (richness = 2, Shannon–Weiner index = 0.17), with oneDaphniagenotype that originated from the most‐eutrophic lake being highly dominant (evenness = 0.25). Thus, eutrophication mediated strong clonal selection of a cyanobacteria‐tolerantDaphniagenotype over just 10 weeks.

    By the end of the experiment,Daphniasignificantly reduced phytoplankton biomass in the high‐nutrient, but not in the low‐nutrient treatment. This difference in effect size was largely driven by the five‐fold higher initial phytoplankton biomass in the high‐nutrient treatment. Thus, the ability ofDaphniato reduce phytoplankton biomass in eutrophic lakes may be driven more so by the abundance of planktivorous fishes, as opposed to the prevalence of cyanobacteria and their associated toxins.

     
    more » « less
  2. Abstract

    Changes in seasonality associated with climate warming (e.g. temperature, growing season duration) are likely to alter invertebrate prey biomass and availability in aquatic ecosystems through direct and indirect influences on physiology and phenology, particularly in arctic lakes. However, despite warmer thermal regimes, photoperiod will remain unchanged such that potential shifts resulting from longer and warmer growing seasons could be limited by availability of sunlight, especially at lower trophic levels. Thus, a better understanding of warming effects on invertebrate prey throughout the growing season (e.g. early, peak, late) is important to understand arctic lake food‐web dynamics in a changing climate.

    Here, we use a multifaceted approach to evaluate prey availability to predators in lakes of arctic Alaska. In a laboratory mesocosm experiment, we measured different metrics of abundance for snails (Lymnaea elodes) and zooplankton (Daphnia middendorffiana) across three time periods (early, mid‐ and late growing season) and across three temperature and photoperiod treatments (control, increased temperature and increased temperature × photoperiod). Additionally, we used generalised additive models and generalised additive mixed‐effects models to relate long‐term empirical observations of zooplankton biomass (1983–2015) to observed temperature regimes in an arctic lake. We then simulated zooplankton biomass for the warmest temperature observations across the growing season to inform likely zooplankton biomass regimes under future change.

    We observed variable responses by snails and zooplankton across experiments and treatments. Early in the growing season, snail development was accelerated at multiple life stages (e.g. egg and juvenile). In mid‐season, in accordance with warmer temperatures, we observed significantly increasedDaphniaabundances. However, in the late season,Daphniaappeared to be limited by photoperiod. Confirming our experimental results, our models of zooplankton biomass showed an increase of nearly 20% in warmer years. Further, these model estimates could be conservative as the consumptive demand of fishes may increase in warmer years as well.

    Overall, our results highlight the importance of interactive effects of temperature and seasonality. Based primarily on temperature, we can readily predict the response of fish metabolism in warmer temperatures. However, in this context, we generally require a better understanding of climate‐driven responses of important invertebrate prey resources. Our results suggest invertebrate prey biomass and availability are likely to respond positively with climate change based on temperature and seasonality, as well as proportionally to the metabolic requirements of fish predators. While further research is necessary to understand how other food‐web components will respond climate change, our findings suggest that the fish community at the top of arctic lake food webs will have adequate prey base in a warming climate.

     
    more » « less
  3. Abstract

    Increases in nitrogen (N) and phosphorus (P) availability are changing animal communities, partly by altering stoichiometric imbalances between consumers and their food. Testing relationships between resource stoichiometry and consumer assemblage structure requires ecosystem‐level manipulations that have been lacking to date.

    We analysed patterns of macroinvertebrate community composition in five detritus‐based headwater streams subject to experimental whole‐stream N and P additions that spanned a steep gradient in dissolved N:P ratio (2:1, 8:1, 16:1, 32:1, 128:1) over 2 years, following a 1‐year pre‐treatment period.

    We predicted that shifts in leaf litter stoichiometry would drive overall patterns of community composition via greater responses of shredders to enrichment than other taxa, as shredders dominate primary consumer biomass and experience larger consumer–resource elemental imbalances than other functional groups in stream ecosystems. Specifically, we expected litter C:P to be a significant predictor of shredder biomass given the greater relative imbalances between shredder and litter C:P than C:N. Finally, we tested whether shredder responses to enrichment were related to other taxon‐level traits, including body size and stoichiometry, larval life span and growth rate.

    Whole‐community composition shifted similarly across the five streams after enrichment, largely driven by increased shredder and predator biomass. These shifts were limited to the autumn/winter seasons and related to decreased leaf litter C:P, highlighting important links between the quality of seasonal litter subsidies and community phenology.

    Among 10 taxa that drove structural shifts, two declined while other taxa from the same functional/taxonomic groups responded positively, suggesting that specific life‐history traits may determine sensitivity to enrichment.

    Increases in total shredder biomass, and in biomass of several common shredders, were associated with lower litter C:P. Body C:P did not predict shredder response to enrichment. However, weak negative relationships between shredder response and body size, and larval life span, suggest that small‐bodied and short‐lived taxa may be more responsive to shifting resource stoichiometry.

    Moderate anthropogenic increases in N and P availability affect resource stoichiometry and can alter animal communities, influencing additional food web and ecosystem properties. We provide support for ecological stoichiometry as a framework for predicting such outcomes based on changes in the elemental composition of resource pools.

    Aplain language summaryis available for this article.

     
    more » « less
  4. Abstract

    In streams, unionoid mussels and fish form aggregations that exert bottom‐up and top‐down effects on food webs, but the magnitude and spatial extent of their effects are controlled by species traits. Sedentary mussels live burrowed in the sediment in patchily distributed dense aggregations (mussel beds) where they filter seston and provide a local, relatively constant nutrient subsidy. In contrast, fish move on and off mussel beds, and thus comprise a transient nutrient subsidy.

    We asked how overlap between fish and mussels influences nutrient recycling and resource distribution in streams. We conducted an 8‐week study in experimental streams where we created mussel beds (comprised of two species,Actinonaias ligamentinaandAmblema plicata), manipulated the occurrence of a grazing minnow (Campostoma anomalum), and tracked nutrient (nitrogen and phosphorus) and resource (algae, detritus, and chironomids) abundance up and downstream of the mussel beds.

    In general, neither consumer had strong effects on the concentration or spatial distribution of nutrients. Water turnover time in our experimental streams may have diluted fish and mussel nutrient excretion effects, making it difficult to detect spatial patterns during a given sampling period.

    Fish controlled the abundance and productivity of algae. In treatments without fish, large mats of filamentous algae formed early in the experiment. These algae senesced, decomposed, and were not replaced. When fish were present, algae consisted of attached biofilms with consistent biomass and spatial distribution over time.

    Although previous work has shown that mussels can have strong, seasonal bottom‐up effects on both primary and secondary production, our results suggested that adding grazing mobile fishes, led to a more consistent and homogenous supply of algal resources. Because mussels rarely occur in the absence of fish, considering their combined influence on ecosystem dynamics is likely to be important.

     
    more » « less
  5. Abstract

    Snake River Sockeye SalmonOncorhynchus nerka, listed as an endangered species in 1991, currently inhabit three nursery lakes (Redfish, Pettit, and Alturas lakes) in the Sawtooth Valley, Idaho. Conspecific kokanee (lacustrine Sockeye Salmon) are also present in the lakes. Snake River Sockeye Salmon recovery efforts, initially focused on genetic conservation, are now attempting to rebuild naturally spawning populations using hatchery supplementation. However, in Sockeye Salmon nursery lakes, density dependence is frequently observed when elevatedO. nerkaabundance leads to declines in zooplankton biomass, body size, and shifts in community composition. In turn, these changes lead to reductions in juvenileO. nerkagrowth rates, survival, and adult returns. We examined a long‐term data set ofO. nerkapopulation metrics and associated zooplankton community metrics. We found evidence of density dependence within and among nursery lakes. We detected differences in zooplankton biomass, lengths of preferred zooplankton prey (Daphniaspp. and cyclopoid copepods), parr growth rates, and age‐1 smolt size among the three lakes. We found negative relationships betweenO. nerkadensity and zooplankton biomass and size. We identified positive relationships between zooplankton biomass and two response variables: smolt size at migration and growth rates of hatchery parr. The relationships were generally similar among lakes. Variable outcomes were a result of differences inO. nerkadensity (or zooplankton biomass), controlled primarily by the relative proportion of spawning and rearing habitat in each lake. Understanding unique lake habitats, ecological interactions, and the role of density dependence is germane to management of Snake River Sockeye Salmon populations.

     
    more » « less