Resolving 500 Years of Anthropogenic Impacts in a Mesotrophic Lake: Nutrients Outweigh Other Drivers of Lake Change.

Interactions among multiple stressors, legacies of past perturbations, and the lack of historical information make it difficult to determine the influence of individual anthropogenic impacts on lakes and separate them from natural ecosystem variability. In the present study, we coupled paleolimnological approaches, historical data, and ecological experiments to disentangle the impacts of multiple long-term stressors on lake ecosystem structure and function. We found that the lake structure and function remained resistant to the impacts of catchment deforestation and erosion, and the introduction of several exotic fish species. Changes in ecosystem structure and function were consistent, with nutrient enrichment being the primary driver of change. Significant and sustained changes in the lake diatom community structure (and their nutrient requirements), bacterial community function, and paleolimnological proxies of ecosystem function coincided with nitrogen and phosphorus fertilizers in the catchment. The results highlight that the effects of increased nutrient inputs are much stronger than the influence of other, potentially significant, drivers of ecosystem change, and that the degree of nutrient impact can be underestimated by environmental monitoring due to its diffuse and accumulative nature. Delineating the effects of multiple anthropogenic drivers requires long-term records of both impacts and lake ecosystem change across multiple trophic levels.

Lake microbial communities are not resistant or resilient to repeated large-scale natural pulse disturbances.

Opportunities to study community-level responses to extreme natural pulse disturbances in unaltered ecosystems are rare. Lake sediment records that span thousands of years can contain well-resolved sediment pulses, triggered by earthquakes. These palaeorecords provide a means to study repeated pulse disturbances and processes of resistance (insensitivity to disturbance) and ecological resilience (capacity to regain structure, function and process). In this study, sedimentary DNA was extracted from a sediment core from Lake Paringa (New Zealand) that is situated in a near natural catchment. Metabarcoding and inferred functions were used to assess the lake microbial community over the past 1100 years - a period that included four major earthquakes. Microbial community composition and function differed significantly between highly perturbed (postseismic, ~50 years) phases directly after the earthquakes and more stable (interseismic, ~250 years) phases, indicating a lack of community resistance. Although community structure differed significantly in successive postseismic phases, function did not, suggesting potential functional redundancy. Significant differences in composition and function in successive interseismic phases demonstrate that communities are not resilient to large-scale natural pulse disturbances. The clear difference in structure and function, and high number of indicator taxa (responsible for driving differences in communities between phases) in the fourth interseismic phase probably represents a regime shift, possibly due to the two-fold increase in sediment and terrestrial biospheric organic carbon fluxes recorded following the fourth earthquake. Large pulse disturbances that enhance sediment inputs into lake systems may produce an underappreciated mechanism that destabilises lake ecosystem processes.

Recent warming reduces the reproductive advantage of large size and contributes to evolutionary downsizing in nature.

Body size is a key functional trait that is predicted to decline under warming. Warming is known to cause size declines via phenotypic plasticity, but evolutionary responses of body size to warming are poorly understood. To test for warming-induced evolutionary responses of body size and growth rates, we used populations of mosquitofish (Gambusia affinis) recently established (less than 100 years) from a common source across a strong thermal gradient (19-33°C) created by geothermal springs. Each spring is remarkably stable in temperature and is virtually closed to gene flow from other thermal environments. Field surveys show that with increasing site temperature, body size distributions become smaller and the reproductive advantage of larger body size decreases. After common rearing to reveal recently evolved trait differences, warmer-source populations expressed slowed juvenile growth rates and increased reproductive effort at small sizes. These results are consistent with an adaptive basis of the plastic temperature-size rule, and they suggest that temperature itself can drive the evolution of countergradient variation in growth rates. The rapid evolution of reduced juvenile growth rates and greater reproduction at a small size should contribute to substantial body downsizing in populations, with implications for population dynamics and for ecosystems in a warming world.

Prey adaptation along a competition-defense tradeoff cryptically shifts trophic cascades from density- to trait-mediated.

Trophic cascades have become a dominant paradigm in ecology, yet considerable debate remains about the relative strength of density- (consumptive) and trait-mediated (non-consumptive) effects in trophic cascades. This debate may, in part, be resolved by considering prey experience, which shapes prey traits (through genetic and plastic change) and influences prey survival (and therefore density). Here, we investigate the cascading role of prey experience through the addition of mosquitofish (Gambusia affinis) from predator-experienced or predator-naïve sources to mesocosms containing piscivorous largemouth bass (Micropterus salmoides), zooplankton, and phytoplankton. These two sources were positioned along a competition-defense tradeoff. Results show that predator-naïve mosquitofish suffered higher depredation rates, which drove a density-mediated cascade, whereas predator-experienced mosquitofish exhibited higher survival but fed less, which drove a trait-mediated cascade. Both cascades were similar in strength, leading to indistinguishable top-down effects on lower trophic levels. Therefore, the accumulation of prey experience with predators can cryptically shift cascade mechanisms from density- to trait-mediated.

Local adaptation reduces the metabolic cost of environmental warming.

Metabolism shapes the ecosystem role of organisms by dictating their energy demand and nutrient recycling potential. Metabolic theory (MTE) predicts consumer metabolic and recycling rates will rise with warming, especially if body size declines, but it ignores potential for adaptation. We measured metabolic and nutrient excretion rates of individuals from populations of a globally invasive fish that colonized sites spanning a wide temperature range (19-37°C) on two continents within the last 100 yr. Fish body size declined across our temperature gradient and MTE predicted large rises in population energy demand and nutrient recycling. However, we found that the allometry and temperature dependency of metabolism varied in a countergradient pattern with local temperature in a way that offset predictions of MTE. Scaling of nutrient excretion was more variable and did not track temperature. Our results suggest that adaptation can reduce the metabolic cost of warming, increasing the prospects for population persistence under extreme warming scenarios.

Drivers of nitrogen transfer in stream food webs across continents.

Studies of trophic-level material and energy transfers are central to ecology. The use of isotopic tracers has now made it possible to measure trophic transfer efficiencies of important nutrients and to better understand how these materials move through food webs. We analyzed data from thirteen 15 N-ammonium tracer addition experiments to quantify N transfer from basal resources to animals in headwater streams with varying physical, chemical, and biological features. N transfer efficiencies from primary uptake compartments (PUCs; heterotrophic microorganisms and primary producers) to primary consumers was lower (mean 11.5%, range <1% to 43%) than N transfer efficiencies from primary consumers to predators (mean 80%, range 5% to >100%). Total N transferred (as a rate) was greater in streams with open compared to closed canopies and overall N transfer efficiency generally followed a similar pattern, although was not statistically significant. We used principal component analysis to condense a suite of site characteristics into two environmental components. Total N uptake rates among trophic levels were best predicted by the component that was correlated with latitude, DIN:SRP, GPP:ER, and percent canopy cover. N transfer efficiency did not respond consistently to environmental variables. Our results suggest that canopy cover influences N movement through stream food webs because light availability and primary production facilitate N transfer to higher trophic levels.

Population divergence in fish elemental phenotypes associated with trophic phenotypes and lake trophic state.

Studies of ecological stoichiometry typically emphasize the role of interspecific variation in body elemental content and the effects of species or family identity. Recent work suggests substantial variation in body stoichiometry can also exist within species. The importance of this variation will depend on insights into its origins and consequences at various ecological scales, including the distribution of elemental phenotypes across landscapes and their role in nutrient recycling. We investigated whether trophic divergence can produce predictable patterns of elemental phenotypes among populations of an invasive fish, the white perch (Morone americana), and whether elemental phenotypes predict nutrient excretion. White perch populations exhibited a gradient of trophic phenotypes associated with landscape-scale variation in lake trophic state. Perch body chemistry varied considerably among lakes (from 0.09 for % C to 0.31-fold for % P) casting doubt on the assumption of homogenous elemental phenotypes. This variation was correlated with divergence in fish body shape and other trophic traits. Elemental phenotypes covaried (r (2) up to 0.84) with lake trophic state. This covariation likely arose in contemporary time since many of these perch populations were introduced in the last century and the trophic state in many of the lakes has changed in the past few decades. Nutrient excretion varied extensively among populations, but was not readily related to fish body chemistry or lake trophic state. This suggests that predictable patterns of fish body composition can arise quickly through trophic specialization to lake conditions, but such elemental phenotypes may not translate to altered nutrient recycling by fish.

Multigenerational exposure to increased temperature reduces metabolic rate but increases boldness in Gambusia affinis.

Acute exposure to warming temperatures increases minimum energetic requirements in ectotherms. However, over and within multiple generations, increased temperatures may cause plastic and evolved changes that modify the temperature sensitivity of energy demand and alter individual behaviors. Here, we aimed to test whether populations recently exposed to geothermally elevated temperatures express an altered temperature sensitivity of metabolism and behavior. We expected that long-term exposure to warming would moderate metabolic rate, reducing the temperature sensitivity of metabolism, with concomitant reductions in boldness and activity. We compared the temperature sensitivity of metabolic rate (acclimation at 20 vs. 30°C) and allometric slopes of routine, standard, and maximum metabolic rates, in addition to boldness and activity behaviors, across eight recently divergent populations of a widespread fish species (Gambusia affinis). Our data reveal that warm-source populations express a reduced temperature sensitivity of metabolism, with relatively high metabolic rates at cool acclimation temperatures and relatively low metabolic rates at warm acclimation temperatures compared to ambient-source populations. Allometric scaling of metabolism did not differ with thermal history. Across individuals from all populations combined, higher metabolic rates were associated with higher activity rates at 20°C and bolder behavior at 30°C. However, warm-source populations displayed relatively bolder behavior at both acclimation temperatures compared to ambient-source populations, despite their relatively low metabolic rates at warm acclimation temperatures. Overall, our data suggest that in response to warming, multigenerational exposure (e.g., plasticity, adaptation) may not result in trait change directed along a simple "pace-of-life syndrome" axis, instead causing relative decreases in metabolism and increases in boldness. Ultimately, our data suggest that multigenerational warming may produce a novel combination of physiological and behavioral traits, with consequences for animal performance in a warming world.

Disentangling the influence of microplastics and their chemical additives on a model detritivore system.

Microplastics (MPs) can negatively impact freshwater organisms via physical effects of the polymer itself and/or exposure to chemicals added to plastic during production to achieve desired characteristics. Effects on organisms may result from direct exposure to plastic particles and/or chemical additives or effects may manifest as indirect effects through ecological interactions between organisms (e.g., reduced food availability that impairs a consumer). To disentangle these issues, we used a simplified freshwater food web interaction comprising microbes and macroinvertebrate detritivores to evaluate the toxicity of 1) polyvinyl chloride (PVC) MPs without added chemicals (virgin), 2) the common chemical additive dibutyl phthalate (DBP), and 3) PVC MPs with incorporated DBP. Exposure to virgin PVC MPs (0.33 and 3.3 mg/L) caused negligible ecological effect with the exception of reduced macroinvertebrate feeding rates at 3.3 mg/L. Exposure to DBP (1 mg/L) both individually and when incorporated into the PVC MPs negatively impacted all tested endpoints, including microbial and macroinvertebrate respiration, feeding rate and assimilation efficiency. DBP leached rapidly from the MPs into the water, and also accumulated in macroinvertebrates and their food, providing multiple routes of exposure. Our findings suggest that additives which are intentionally incorporated into MPs could play a key role in MP toxicity and contribute to the disruption of key ecological interactions underpinning ecosystem processes, such as leaf litter decomposition.

A bacterial index to estimate lake trophic level: National scale validation.

Lakes and their catchments have been subjected to centuries to millennia of exploitation by humans. Efficient monitoring methods are required to promote proactive protection and management. Traditional monitoring is time consuming and expensive, which limits the number of lakes monitored. Lake surface sediments provide a temporally integrated representation of environmental conditions and contain high microbial biomass. Based on these attributes, we hypothesized that bacteria associated with lake trophic states could be identified and used to develop an index that would not be confounded by non-nutrient stressor gradients. Metabarcoding (16S rRNA gene) was used to assess bacterial communities present in surface sediments from 259 non-saline lakes in New Zealand encompassing a range of trophic states from alpine microtrophic lakes to lowland hypertrophic lakes. A subset of lakes (n = 96) with monitoring data was used to identify indicator amplicon sequence variants (ASVs) associated with different trophic states. A total of 10,888 indicator taxa were identified and used to develop a Sediment Bacterial Trophic Index (SBTI), which signficantly correlated (r2 = 0.842, P < 0.001) with the Trophic Lake Index. The SBTI was then derived for the remaining 163 lakes, providing new knowledge of the trophic state of these unmonitored lakes. This new, robust DNA-based tool provides a rapid and cost-effective method that will allow a greater number of lakes to be monitored and more effectively managed in New Zealand and globally. The SBTI could also be applied in a paleolimnological context to investigate changes in trophic status over centuries to millennia.

Towards more ecologically relevant investigations of the impacts of microplastic pollution in freshwater ecosystems.

Microplastic pollution is a major environmental concern and the subject of a rapidly growing body of research. Much of this research has focused on the direct effects of microplastics on single species and there is limited information on how microplastics affect different functional groups of organisms, multi-species interactions, and ecosystem processes. We focused on freshwater systems and reviewed 146 studies of microplastic effects on freshwater biota and recorded features including particle characteristics, study designs, functional types of species tested and ecotoxicological endpoints measured. Study species were categorized based on their ecosystem role/functional feeding group rather than taxonomy. We found that most studies were conducted on single species (95%) and focused on a narrow range of functional groups of organisms (mostly filter feeders, 37% of studies). Very few studies have investigated multi-species interactions and ecosystem processes. In many studies, certain characteristics of microplastics, such as polymer type were not well matched with the feeding and habitat ecology of test species, potentially reducing their ecological relevance. Median laboratory study test concentrations were 5-6 orders of magnitude higher than those reported in the field and few studies considered the effects of chemical additives in plastics (6%). We recommend that studies addressing the ecological effects of microplastics need to address neglected functional groups of organisms, design experiments to better match the ecology of test species, and increase in experimental scale and complexity to identify any indirect effects on species interactions and ecosystem processes. We suggest that examining microplastics through an ecological lens that better integrates the feeding and habitat ecology of test organisms will advance our understanding of the effects microplastics have in the environment.

Stream ecosystem response to chronic deposition of N and acid at the Bear Brook Watershed, Maine.

The Bear Brook Watershed in Maine (BBWM) is a long-term, paired watershed experiment that addresses the effects of acid and nitrogen (N) deposition on whole watersheds. To examine stream response at BBWM, we synthesized data on organic matter dynamics, including leaf breakdown rates, organic matter inputs and standing stocks, macroinvertebrate secondary production, and nutrient uptake in treated and reference streams at the BBWM. While N concentrations in stream water and leaves have increased, the input, standing stocks, and breakdown rates of leaves, as well as macroinvertebrate production, were not responsive to acid and N deposition. Both chronic and acute increases of N availability have saturated uptake of nitrate in the streams. Recent experimental increases in phosphorus (P) availability enhanced stream capacity to take up nitrate and altered the character of N saturation. These results show how the interactive effects of multiple factors, including environmental flow regime, acidification, and P availability, may constrain stream response to chronic N deposition.

Influence of dissolved organic matter and invertebrates on the function of microbial films in groundwater.

Microbial films play a central role in mediating energy flux in groundwater ecosystems. The activity of these microbes is likely to be influenced by the availability of resources, especially dissolved organic matter (DOM), and also by consumers, such as invertebrates that feed on microbial films. We used microcosm experiments to examine how bacterial production and extracellular enzyme activity on rocks and fine sediments from cave streams responded to amendments of DOM of varying form and to cave amphipods (Gammarus minus) that feed on microbial films. Glucose and mixtures of DOM extracted from soils and leaves stimulated bacterial production on rocks by 89-166% relative to unamended controls. In contrast, tannic acid amendment did not influence production. Microbial films on fine sediment were not consistently responsive to DOM amendment. Glucose amendment led to increased activity of enzymes associated with C acquisition, but other forms of DOM generally did not alter enzyme activity. DOM amendment led to removal of nitrate and this was correlated with bacterial production, suggesting microbes can link carbon and nitrogen cycling in groundwater as is the case in surface systems. Amphipods reduced bacterial production on rocks, but not fine sediments. The reduction caused by amphipods offset the stimulatory effect of glucose amendment, but there was no interactive effect of DOM and grazing on bacterial production or enzyme activity. Both resources and consumers play important roles in regulating microbial activity in groundwater with important implications for higher trophic levels that use microbes for food.

Microplastic pollution in streams spanning an urbanisation gradient.

Microplastic pollution has received considerable attention in marine systems, but recent work shows substantial plastic pollution also occurs in freshwater ecosystems. Most freshwater research has focused on large rivers and lakes, but small streams are the primary interface between land, where plastic is used, and drainage networks. We examined variation in the amount and form of plastic occurring in small streams spanning an urbanisation gradient. All streams contained microplastics with concentrations similar to that found in larger systems (up to 303 particles m-3 in water and 80 particles kg-1 in sediment). The most abundant types were fragments and small particles (63-500 µm). Chemical types of plastic were quite variable and often not predictable based on size, form and colour. Variation in microplastic abundance across streams was high, but only partially explained by catchment scale parameters. There was no relationship between human population density or combined stormwater overflows and microplastic abundance. Residential land cover was related to microplastic abundance, but explanatory power was low. Our results suggest local-scale factors may be more important than catchment-scale processes in determining microplastic pollution in small streams.

Increasing agricultural land use is associated with the spread of an invasive fish (Gambusia affinis).

Land-use change and invasive species pose major threats to ecosystems globally. These stressors can act together, with disturbance due to changes in land-use facilitating invasion. We examined the potential for agricultural land use to facilitate the establishment and population growth (abundance) of a globally invasive fish (Gambusia affinis). To achieve this we examined Gambusia presence, abundance, and life history traits in 31 streams spanning an agricultural land use gradient in the North Island of New Zealand. We used regression models to quantify the relationship between agricultural land use and in-stream physiochemical and habitat variables, and zero-inflated models to explore the relationship among physiochemical, habitat and catchment-scale variables and Gambusia's distribution and abundance. The percentage of the catchment in agricultural land use was associated with changes to physiochemical and habitat conditions. Increasing agricultural land use was associated with increasing macrophyte cover and water temperature and decreasing velocity in streams. Catchment-scale variables (land use and site position in the network) and water temperature were the most important determinants of whether Gambusia occurred at a site. Local in-stream habitat (macrophyte cover and water velocity) and nutrient conditions were the most influential predictors of Gambusia abundance given Gambusia were present. Gambusia life-history traits, sex ratio and body length varied among sites but were not predicted by physiochemical gradients. The distribution of Gambusia in streams in New Zealand is partially controlled by catchment-scale conditions via a combination of dispersal limitation and environmental filtering, both of which are affected by agricultural land use. Agricultural land use alters local in-stream conditions, resulting in systems that are similar to those in Gambusia's natural range; these altered systems have the potential to support an increased abundance of Gambusia. This study provides preliminary quantitative evidence that agricultural land use is related to the spread of a globally invasive freshwater fish.