Net effects of multiple stressors in freshwater ecosystems: a meta‐analysis

The accelerating rate of global change has focused attention on the cumulative impacts of novel and extreme environmental changes (i.e. stressors), especially in marine ecosystems. As integrators of local catchment and regional processes, freshwater ecosystems are also ranked highly sensitive to the net effects of multiple stressors, yet there has not been a large‐scale quantitative synthesis. We analysed data from 88 papers including 286 responses of freshwater ecosystems to paired stressors and discovered that overall, their cumulative mean effect size was less than the sum of their single effects (i.e. an antagonistic interaction). Net effects of dual stressors on diversity and functional performance response metrics were additive and antagonistic, respectively. Across individual studies, a simple vote‐counting method revealed that the net effects of stressor pairs were frequently more antagonistic (41%) than synergistic (28%), additive (16%) or reversed (15%). Here, we define a reversal as occurring when the net impact of two stressors is in the opposite direction (negative or positive) from that of the sum of their single effects. While warming paired with nutrification resulted in additive net effects, the overall mean net effect of warming combined with a second stressor was antagonistic. Most importantly, the mean net effects across all stressor pairs and response metrics were consistently antagonistic or additive, contrasting the greater prevalence of reported synergies in marine systems. Here, a possible explanation for more antagonistic responses by freshwater biota to stressors is that the inherent greater environmental variability of smaller aquatic ecosystems fosters greater potential for acclimation and co‐adaptation to multiple stressors.     

Trophic status determines the nirS-denitrifier community in shallow freshwater lakes

To explore whether trophic status is involved in identifying the denitrifier communities in shallow freshwater lakes, comparative studies regarding the variation of nirS-denitrifier communities were performed in water columns of six shallow freshwater lakes, ranging from mesotrophic to hypereutrophic status, in Jiangsu province of China. Restriction fragment length polymorphism (RFLP) analysis and cloning, followed by sequence analysis of selected samples were performed to examine the nirS-denitrifier communities. Results showed that a same predominant nirS unique operational taxonomic unit (OTU) appeared in mesotrophic, light eutrophic and middle eutrophic lakes, while a different nirS OTU appeared in the hypereutrophic lake. The nirS dendrogram could be divided into four clusters, and suggested a habitat-specific observation. The nirS libraries from lakes having mesotrophic and light eutrophic statuses grouped together, while those from lakes having middle eutrophic and hypereutrophic statuses diverged. The hypereutrophic lake had the lowest richness and evenness of nirS. Thus, the observed variation of nirS distribution and diversity was mainly affected by the trophic status, via some environmental factors such as pH, dissolved oxygen, nitrite, nitrate and chlorophyll-a concentrations.     

How important are trophic state,macrophyte and fish population effects on cladoceran community? A study in Lake Erhai

Environmental controls on cladoceran community structure in lake ecosystems are complex and may involve many environmental parameters including trophic state and fish populations. In Lake Erhai, a plateau lake located in southwest China, it was hypothesized that a combination of lake eutrophication and planktivorous fish introduction would increase the abundance of cladoceran, while also decreasing cladoceran size. To test this hypothesis, we examined temporal changes in cladoceran microfossils in the sediments of Lake Erhai over the past century. The influence of changing macrophyte coverage within the littoral region of the lake was also considered. Results demonstrated that cladoceran abundance (measured as flux of cladoceran fossils in the sediments) increased markedly accompanying eutrophication of the lake. In addition, there was a shift in the dominant cladoceran species from those species that prefer oligotrophic conditions to those that prefer mesotrophic and eutrophic conditions. A reduction in the ephippium length of Daphnia spp. was observed and attributed to the introduction of the planktivorous fish Neosalanx taihuensis. Our findings indicated that eutrophication and fish introduction were the main controls affecting cladoceran community structure during the recent decades, and predation by planktivorous fish had an important impact on Daphnia body size.     

No evidence for a cost of selection by carbaryl exposure in terms of vulnerability to fish predation in <Emphasis Type="Italic">Daphnia magna</Emphasis>

Natural populations are exposed to multiple stressors. These stressors may interact, leading to synergistic or antagonistic responses. In addition to these direct interaction effects, there may also be an interaction between stressors through a selection effect: as the population genetically responds to one stressor, it may become more vulnerable to another one, for instance because of an associated reduction in genetic variation. We here capitalized on a selection experiment involving the exposure of Daphnia populations to carbaryl pulses to test the hypothesis that selection imposed by this pesticide may increase vulnerability to fish predation in the resulting population. A direct predation experiment with individuals isolated from carbaryl-exposed and non-exposed populations revealed no effect of prior selection by carbaryl exposure on mortality due to stickleback predation.     

Managing for Interactions between Local and Global Stressors of Ecosystems

Global stressors, including climate change, are a major threat to ecosystems, but they cannot be halted by local actions. Ecosystem management is thus attempting to compensate for the impacts of global stressors by reducing local stressors, such as overfishing. This approach assumes that stressors interact additively or synergistically, whereby the combined effect of two stressors is at least the sum of their isolated effects. It is not clear, however, how management should proceed for antagonistic interactions among stressors, where multiple stressors do not have an additive or greater impact. Research to date has focussed on identifying synergisms among stressors, but antagonisms may be just as common. We examined the effectiveness of management when faced with different types of interactions in two systems – seagrass and fish communities – where the global stressor was climate change but the local stressors were different. When there were synergisms, mitigating local stressors delivered greater gains, whereas when there were antagonisms, management of local stressors was ineffective or even degraded ecosystems. These results suggest that reducing a local stressor can compensate for climate change impacts if there is a synergistic interaction. Conversely, if there is an antagonistic interaction, management of local stressors will have the greatest benefits in areas of refuge from climate change. A balanced research agenda, investigating both antagonistic and synergistic interaction types, is needed to inform management priorities.     

Tolerance to Copper and to Salinity in Daphnia longispina: Implications within a Climate Change Scenario

Considering IPPC climate change scenarios, it is pertinent to predict situations where coastal ecosystems already impacted with chemical contamination became exposed to an additional stressor under a future scenario of seawater intrusion. Accordingly, the present study aimed at evaluating if a negative association between tolerance to a metal and to saltwater exists among genotypes of a freshwater organism. For this, five clonal lineages of the cladoceran Daphnia longispina O.F. Müller, exhibiting a differential tolerance to lethal levels of copper, were selected. Each clonal lineage was exposed to lethal and sublethal concentrations of sodium chloride (assumed as a protective surrogate to evaluate the toxicity of increased salinity to freshwater organisms). Mortality, time to release the first brood and total number of neonates per female were monitored and the somatic growth rate and intrinsic rate of natural increase were computed for each clonal lineage. Data here obtained were compared with their lethal responses to copper and significant negative correlations were found. These results suggest that genetically eroded populations of D. longispina, due to copper or salinity, may be particularly susceptible to a later exposure to the other contaminant supporting the multiple stressors differential tolerance.     

The role of meiobenthos in lake ecosystems

It is shown that meiobenthos plays an important role in the secondary production by zoobenthos in lakes, as well as in the degradation of organic matter. In large lakes (Lake Ladoga, Lake Onega, Lake Päijänne, Lake Constance), the ratio of meiobenthic production to the production of macrobenthos is on average 50–61%. In the small Latgalian lakes (Latvia), this proportion is different: in the profundal of these lakes it varies from 92.5% in a naturally clean mesotrophic lake to 0.0004% in the most eutrophic lake, and in the littoral of lakes – from 578–1476% in mesotrophic lakes to 148–306% in eutrophic ones. The level of production of littoral meiobenthos does not depend on the trophic status of the lake, and can be equally high both in undisturbed mesotrophic lakes and in strongly eutrophicated lakes. The intensity of production of the littoral meiobenthos in oligotrophic and mesotrophic lakes, on the one hand, and in eutrophic lakes on the other, are not reliably distinguished. There is a clear tendency for a decrease of the role of profundal meiobenthos with regard to the transformation of energy flows in lake ecosystems, both with an increase in eutrophication and with an increase in the amount of organic matter in the benthal available from phytoplankton.     

The enemy of my enemy is my friend: intraguild predation between invaders and natives facilitates coexistence with shared invasive prey

Understanding and predicting the outcomes of biological invasions is challenging where multiple invader and native species interact. We hypothesize that antagonistic interactions between invaders and natives could divert their impact on subsequent invasive species, thus facilitating coexistence. From field data, we found that, when existing together in freshwater sites, the native amphipod Gammarus duebeni celticus and a previous invader G. pulex appear to facilitate the establishment of a second invader, their shared prey Crangonyx pseudogracilis. Indeed, the latter species was rarely found at sites where each Gammarus species was present on its own. Experiments indicated that this may be the result of G. d. celticus and G. pulex engaging in more intraguild predation (IGP) than cannibalism; when the ‘enemy’ of either Gammarus species was present, that is, the other Gammarus species, C. pseudogracilis significantly more often escaped predation. Thus, the presence of mutual enemies and the stronger inter- than intraspecific interactions they engage in can facilitate other invaders. With some invasive species such as C. pseudogracilis having no known detrimental effects on native species, and indeed having some positive ecological effects, we also conclude that some invasions could promote biodiversity and ecosystem functioning.     

Predators modify the evolutionary response of prey to temperature change

As climate regimes shift in many ecosystems worldwide, evolution may be a critical process allowing persistence in rapidly changing environments. Organisms regularly interact with other species, yet whether climate-mediated evolution can occur in the context of species interactions is not well understood. We tested whether a species interaction could modify evolutionary responses to temperature. We demonstrate that predation pressure by Dipteran larvae (Chaoborus americanus) modified the evolutionary response of a freshwater crustacean (Daphnia pulex) to its thermal environment over approximately seven generations in laboratory conditions. Daphnia kept at 21°C evolved higher population growth rates than those kept at 18°C, but only in those populations that were also reared with predators. Furthermore, predator-mediated selection resulted in the evolution of elevated Daphnia thermal plasticity. This laboratory natural selection experiment demonstrates that biotic interactions can modify evolutionary adaptation to temperature. Understanding the interplay between multiple selective forces can improve predictions of ecological and evolutionary responses of organisms to rapid environmental change.     

Biotic interactions govern genetic adaptation to toxicants

The genetic recovery of resistant populations released from pesticide exposure is accelerated by the presence of environmental stressors. By contrast, the relevance of environmental stressors for the spread of resistance during pesticide exposure has not been studied. Moreover, the consequences of interactions between different stressors have not been considered. Here we show that stress through intraspecific competition accelerates microevolution, because it enhances fitness differences between adapted and non-adapted individuals. By contrast, stress through interspecific competition or predation reduces intraspecific competition and thereby delays microevolution. This was demonstrated in mosquito populations (Culex quinquefasciatus) that were exposed to the pesticide chlorpyrifos. Non-selective predation through harvesting and interspecific competition with Daphnia magna delayed the selection for individuals carrying the ace-1^R resistance allele. Under non-toxic conditions, susceptible individuals without ace-1^R prevailed. Likewise, predation delayed the reverse adaptation of the populations to a non-toxic environment, while the effect of interspecific competition was not significant. Applying a simulation model, we further identified how microevolution is generally determined by the type and degree of competition and predation. We infer that interactions with other species—especially strong in ecosystems with high biodiversity—can delay the development of pesticide resistance.     

Seasonal Variation of Virioplankton in a Eutrophic Shallow Lake

Lake Donghu is a typical eutrophic freshwater lake in which high abundance of planktonic viruses was recently revealed. In this study, seasonal variation of planktonic viruses were observed at three different trophic sites, hypertrophic, eutrophic, and mesotrophic regions, and the correlation between their abundances and other aquatic environmental components, such as bacterioplankton, chlorophyll a, burst size, pH, dissolved oxygen, and temperature, was analyzed for the period of an year. Virioplankton abundance detected by transmission electron microscope (TEM) ranged from 5.48 × 10⁸ to 2.04 × 10⁹ ml⁻¹ in all the sites throughout the study, and the high abundances and seasonal variations of planktonic viruses were related to the trophic status at the sampled sites in Lake Donghu. Their annual mean abundances were, the highest at the hypertrophic site (1.23×10⁹ ml⁻¹), medium at the eutrophic site (1.19×10⁹ ml⁻¹), and the lowest at the mesotrophic site (1.02×10⁹ ml⁻¹). The VBR (virus-to-bacteria ratio) values were high, ranging from 49 to 56 on average at the three sampled sites. The data suggested that the high viral abundance and high VBR values might be associated with high density of phytoplankton including algae and cyanobacteria in this eutrophic shallow lake, and that planktonic viruses are important members of freshwater ecosystems.     

Parasite prevalence in an intermediate snail host is subject to multiple anthropogenic stressors in a New Zealand river system

Most ecosystems are exposed to multiple stressors acting in concert and their combined effects on parasite prevalence in freshwater, marine and terrestrial habitats are largely unknown. We investigated the relationships between farming intensity, water abstraction intensity and parasite prevalence in the mud snail Potamopyrgus antipodarum from 20 stream sites within the Manuherikia River catchment (New Zealand) by using generalized linear models and an information-theoretic model-selection approach. Three trematode taxa that use water birds as definitive hosts were found in the snail host. The average prevalence of all parasites infecting Potamopyrgus in the catchment was 5%. Microphallus sp. “lively”, the most common parasite, was most prevalent at high farming intensity and low water abstraction, besides showing an antagonistic interaction between the two agricultural stressors. These findings highlight the importance of considering multiple stressors and their potential interactions when studying host–parasite systems. Because snails often play key roles in aquatic communities, providing an important link between primary producers and higher trophic levels, and are a common intermediate host to a high diversity of trematode parasites, this host–parasite model system may represent a promising bioassessment tool for detecting anthropogenic disturbances in freshwater systems.     

广东省大中型供水水库营养现状及浮游生物的响应

于2000年调查了广东省18座大中型供水水库的水质现状并探讨了浮游生物对营养水平的响应。总氮、总磷、透明度和叶绿素a分别为0．15～7.15mg／L、0．003～0．387mg／L、0．4～6．3m和0．6～32．3ug／L。总氮、总磷、透明度均与叶绿素a呈较高的相关性。根据这4个因子的综合加权营养状态指数为23．7～55．1,季节差异不大,大多数水库处于中营养状态。金藻在中-富及富营养型水库中没有分布,而蓝藻、绿藻、硅藻和甲藻在调查水库中均有比较广的营养生态位,但它们的密度及相对优势度在各营养型水库中有一定的差异。高营养水平水库有较高的细胞密度和叶绿素a含量。营养水平较低的水库浮游植物以硅藻-甲藻、硅藻-绿藻或金藻-硅藻为主;营养水平较高的水库以蓝藻-硅藻或蓝藻-绿藻为主,并有较高的裸藻密度。浮游动物基本上以桡足类为优势种群,但在中-富营养和富营养型水库中,哲水蚤种类比低营养型水库中少。枝角类优势种类在各营养型水库差别不大。轮虫对水体营养水平的响应相对比较显著。低营养水平水库的轮虫以广营养型、中营养型或寡中营养型种类为主,种类数目比较少;富营养和中-富营养型水库的轮虫以喜在中营养到富营养条件下生长的种类为主,且轮虫种类数目比较多。     

Multiple‐stressor effects on stream invertebrates: a mesocosm experiment manipulating nutrients,fine sediment and flow velocity

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Interactive and cumulative effects of multiple human stressors in marine systems

Humans impact natural systems in a multitude of ways, yet the cumulative effect of multiple stressors on ecological communities remains largely unknown. Here we synthesized 171 studies that manipulated two or more stressors in marine and coastal systems and found that cumulative effects in individual studies were additive (26%), synergistic (36%), and antagonistic (38%). The overall interaction effect across all studies was synergistic, but interaction type varied by response level (community: antagonistic, population: synergistic), trophic level (autotrophs: antagonistic, heterotrophs: synergistic), and specific stressor pair (seven pairs additive, three pairs each synergistic and antagonistic). Addition of a third stressor changed interaction effects significantly in two‐thirds of all cases and doubled the number of synergistic interactions. Given that most studies were performed in laboratories where stressor effects can be carefully isolated, these three‐stressor results suggest that synergies may be quite common in nature where more than two stressors almost always coexist. While significant gaps exist in multiple stressor research, our results suggest an immediate need to account for stressor interactions in ecological studies and conservation planning.     

Biotic interactions modify multiple‐stressor effects on juvenile brown trout in an experimental stream food web

Agricultural land use results in multiple stressors affecting stream ecosystems. Flow reduction due to water abstraction, elevated levels of nutrients and chemical contaminants are common agricultural stressors worldwide. Concurrently, stream ecosystems are also increasingly affected by climate change. Interactions among multiple co‐occurring stressors result in biological responses that cannot be predicted from single‐stressor effects (i.e. synergisms and antagonisms). At the ecosystem level, multiple‐stressor effects can be further modified by biotic interactions (e.g. trophic interactions). We conducted a field experiment using 128 flow‐through stream mesocosms to examine the individual and combined effects of water abstraction, nutrient enrichment and elevated levels of the nitrification inhibitor dicyandiamide (DCD) on survival, condition and gut content of juvenile brown trout and on benthic abundance of their invertebrate prey. Flow velocity reduction decreased fish survival (?12% compared to controls) and condition (?8% compared to initial condition), whereas effects of nutrient and DCD additions and interactions among these stressors were not significant. Negative effects of flow velocity reduction on fish survival and condition were consistent with effects on fish gut content (?25% compared to controls) and abundance of dominant invertebrate prey (?30% compared to controls), suggesting a negative metabolic balance driving fish mortality and condition decline, which was confirmed by structural equation modelling. Fish mortality under reduced flow velocity increased as maximal daily water temperatures approached the upper limit of their tolerance range, reflecting synergistic interactions between these stressors. Our study highlights the importance of indirect stressor effects such as those transferred through trophic interactions, which need to be considered when assessing and managing fish populations and stream food webs in multiple‐stressor situations. However, in real streams, compensatory mechanisms and behavioural responses, as well as seasonal and spatial variation, may alter the intensity of stressor effects and the sensitivity of trout populations.     

Trophic status based on nutrient concentration scales and primary producers community of tropical coastal lagoons influenced by groundwater discharges

Changes in the rate of primary production as an indication of trophic status of aquatic ecosystems have been one of the major indicators of their health. Despite different approaches been devised for evaluating this process, few are useful for comparison and generalization of their results. The coastal zone ecosystems of Yucatan (SE Mexico) exhibit hydrological variability closely associated with the groundwater discharges, which are the only freshwater sources in the coastal ecosystems. In order to learn about the trophic status of karstic tropical coastal lagoons, three of them (Celestun, Chelem and Dzilam) located in Yucatan (SE, Mexico) were monitored for inorganic nutrients, Chl-a, phytoplankton and macrophyte productivity. The nitrate concentrations suggest that the trophic status was influenced by fresh water springs, being meso-eutrophic in Celestun, oligotrophic in Chelem, and mesotrophic in Dzilam. In the case of ammonium ions, the three lagoons were mesotrophic, indicating that processes such as remineralization play an important role in the trophic dynamic of these shallow ecosystems. According to phosphate concentrations, Celestun and Dzilam were mesotrophic, and Chelem was oligotrophic. External inputs of phosphate and bioturbation by waterfowl may be responsible of these differences. Primary productivity at Celestun was greater than at Chelem and Dzilam lagoons and the contribution by seagrasses was significant in all three. It is found that indices based on nutrient concentration and phytoplankton biomass are useful as an indication of trophic status in groundwater influenced coastal lagoons. Moreover, estimations on the total system productivity, and the relative contribution of each primary producer, is a holistic approach useful for understanding trophic dynamic in shallow tropical coastal ecosystems.     

UV radiation affects antipredatory defense traits in Daphnia pulex

In aquatic environments, prey perceive predator threats by chemical cues called kairomones, which can induce changes in their morphology, life histories, and behavior. Predator‐induced defenses have allowed for prey, such as Daphnia pulex, to avert capture by common invertebrate predators, such as Chaoborus sp. larvae. However, the influence of additional stressors, such as ultraviolet radiation (UVR), on the Daphnia–Chaoborus interaction is not settled as UVR may for instance deactivate the kairomone. In laboratory experiments, we investigated the combined effect of kairomones and UVR at ecologically relevant levels on induced morphological defenses of two D. pulex clones. We found that kairomones were not deactivated by UVR exposure. Instead, UVR exposure suppressed induced morphological defense traits of D. pulex juveniles under predation threat by generally decreasing the number of neckteeth and especially by decreasing the size of the pedestal beneath the neckteeth. UVR exposure also decreased the body length, body width, and tail spine length of juveniles, likely additionally increasing the vulnerability to Chaoborus predation. Our results suggest potential detrimental effects on fitness and survival of D. pulex subject to UVR stress, with consequences on community composition and food web structure in clear and shallow water bodies.     

Diversity of the major capsid genes (g23) of T4-like bacteriophages in the eutrophic Lake Kotokel in East Siberia, Russia

Numerous studies revealed high diversity of T4-like bacteriophages in various environments, but so far, little is known about T4-like virus diversity in freshwater bodies, particularly in eutrophic lakes. The present study was aimed at elucidating molecular diversity of T4-like bacteriophages in eutrophic Lake Kotokel located near Lake Baikal by partial sequencing of the major capsid genes (g23) of T4-like bacteriophages. The majority of g23 fragments from Lake Kotokel were most similar to those from freshwater lakes and paddy fields. Despite the proximity and direct water connection between Lake Kotokel and Lake Baikal, g23 sequence assemblages from two lakes were different. UniFrac analysis showed that uncultured T4-like viruses from Lake Kotokel tended to cluster with those from the distant lake of the same trophic status. This fact suggested that the trophic conditions affected the formation of viral populations, particularly of T4-like viruses, in freshwater environments.     

Evidence for consumer regulation of biofilm–nutrient interactions among hardwater streams (Pennsylvania, USA)

Experimental studies evaluating the simultaneous effects of consumers, nutrients, and other biotic/abiotic factors on intact, natural food webs are rare, particularly among ecosystems of varying trophic conditions. We conducted a series of in situ studies that used nutrient-diffusing substrata with nitrogen (N) and phosphorus (P) concentrations in a full factorial design in three temperate, limestone streams in Pennsylvania across a trophic gradient (mesotrophic, eutrophic, and hypereutrophic streams). We assessed differences in algal and macroinvertebrate biomass, taxonomic composition, and functional groups relative to amended nutrients across the trophic gradient; as such, these results facilitated predictions about regulators of food web structure. All factors varied significantly among the streams (e.g., algal biomass P = 0.005, macroinvertebrate biomass P < 0.001, algal diversity P = 0.006, macroinvertebrate diversity P < 0.001, algal group P < 0.001, macroinvertebrate guilds P < 0.001); the streams, however, did not exhibit simple responses to nutrient amendment. Algal and macroinvertebrate biomass and diversity responded greatest in the mesotrophic stream while grazing seemed to be a strong factor preventing algal nutrient response in the eutrophic and hypereutrophic streams. Brillouin’s Evenness Index was most influenced by nutrient amendment (nutrient effect on algae and macroinvertebrates P = 0.021). As such, we concluded that biomass and diversity were mediated by complexity within intermediate trophic levels.