William H. Clements

HEAVY METALS STRUCTURE BENTHIC COMMUNITIES IN COLORADO MOUNTAIN STREAMS

The development of field sampling designs that employ multiple reference and polluted sites has been proposed as an alternative to the traditional upstream vs. down- stream approach used in most biomonitoring studies. Spatially extensive monitoring pro- grams can characterize ecological conditions within an ecoregion and provide the necessary background information to evaluate future changes in water quality. We measured physi- cochemical characteristics, heavy-metal concentrations, and benthic macroinvertebrate com- munity structure at 95 sites in the Southern Rocky Mountain ecoregion in Colorado, USA. Most sites (82%) were selected using a systematic, randomized sampling design. Each site was placed into one of four metal categories (background, low, medium, and high metals), based on the cumulative criterion unit (CCU), which we defined as the ratio of the instream metal concentration to the U.S. Environmental Protection Agency criterion concentration, summed for all metals measured. A CCU of 1.0 represents a conservative estimate of the total metal concentration that, when exceeded, is likely to cause harm to aquatic organisms. Although the CCU was less than 2.0 at most (66.3%) of the sites, values exceeded 10.0 at 13 highly polluted stations. Differences among metal categories were highly significant for most measures of macroinvertebrate abundance and all measures of species richness. We observed the greatest effects on several species of heptageniid mayflies (Ephemeroptera: Heptageniidae), which were highly sensitive to heavy metals and were reduced by .75% at moderately polluted stations. The influence of taxonomic aggregation on responses to metals was also greatest for mayflies. In general, total abundance of mayflies and abundance of heptageniids were better indicators of metal pollution than abundance of dominant mayfly taxa. We used stepwise multiple-regression analyses to investigate the relationship between benthic community measures and physicochemical characteristics at the 78 randomly se- lected sites. Heavy-metal concentration was the most important predictor of benthic com- munity structure at these sites. Because of the ubiquitous distribution of heavy-metal pol- lution in the Southern Rocky Mountain ecoregion, we conclude that potential effects of

Community responses to contaminants: using basic ecological principles to predict ecotoxicological effects.

Community ecotoxicology is defined as the study of the effects of contaminants on patterns of species abundance, diversity, community composition, and species interactions. Recent discoveries that species diversity is positively associated with ecosystem stability, recovery, and services have made a community-level perspective on ecotoxicology more important than ever. Community ecotoxicology must explicitly consider both present and impending global change and shift from a purely descriptive to a more predictive science. Greater consideration of the ecological factors and threshold responses that determine community resistance and resilience should improve our ability to predict how and when communities will respond to, and recover from, xenobiotics. A better understanding of pollution-induced community tolerance, and of the costs of this tolerance, should facilitate identifying contaminant-impacted communities, thus forecasting the ecological consequences of contaminant exposure and determining the restoration effectiveness. Given the vast complexity of community ecotoxicology, simplifying assumptions, such as the possibility that the approximately 100,000 registered chemicals could be reduced to a more manageable number of contaminant classes with similar modes of action, must be identified and validated. In addition to providing a framework for predicting contaminant fate and effects, food-web ecology can help to identify communities that are sensitive to contaminants, contaminants that are particularly insidious to communities, and species that are crucial for transmitting adverse effects across trophic levels. Integration of basic ecological principles into the design and implementation of ecotoxicological research is essential for predicting contaminant effects within the context of rapidly changing, global environmental conditions.

Benthic Invertebrate Community Responses to Heavy Metals in the Upper Arkansas River Basin, Colorado

This research examined effects of heavy metals on benthic macroinvertebrate communities in the upper Arkansas River, Colorado. Benthic macroinvertebrates were collected seasonally (fall, spring, and summer) over a 2-yr period upstream and downstream from two sources of metals, Leadville Mine Drainage Tunnel and California Gulch. Community responses to metals observed in this study were similar to those reported previously for other streams. Benthic communities at reference stations were dominated by mayflies (Ephemeroptera), which generally constituted >50% of the total individuals collected. In contrast, highly polluted and moderately polluted sites were dominated by Orthocladiinae chironomids and caddisflies (Trichoptera); respectively. The spatial distribution of specific taxa at the Arkansas River was influenced by several factors, including their tolerance for heavy metals, their recolonization ability, and natural environmental conditions. Distribution patterns of some groups (e.g., mayflies, stoneflies, beetles, and Orthocladiinae chironomids) appeared to be directly affected by heavy metals, whereas the distribution of other groups (e.g., caddisflies and black flies) was probably more influenced by factors such as food availability. Macroinvertebrate community responses to metals were complicated by natural seasonal and longitudinal changes in community composition. The greatest effects on community composition and abundance of sensitive taxa were observed during spring, when metal levels were highest. Some longitudinal changes in species richness and abundance of dominant taxa were independent of heavy metals. Determination of the effects of heavy metals on benthic communities requires careful evaluation of natural changes in community composition.

Combined and interactive effects of global climate change and toxicants on populations and communities

Increased temperature and other environmental effects of global climate change (GCC) have documented impacts on many species (e.g., polar bears, amphibians, coral reefs) as well as on ecosystem processes and species interactions (e.g., the timing of predator–prey interactions). A challenge for ecotoxicologists is to predict how joint effects of climatic stress and toxicants measured at the individual level (e.g., reduced survival and reproduction) will be manifested at the population level (e.g., population growth rate, extinction risk) and community level (e.g., species richness, food-web structure). The authors discuss how population- and community-level responses to toxicants under GCC are likely to be influenced by various ecological mechanisms. Stress due to GCC may reduce the potential for resistance to and recovery from toxicant exposure. Long-term toxicant exposure can result in acquired tolerance to this stressor at the population or community level, but an associated cost of tolerance may be the reduced potential for tolerance to subsequent climatic stress (or vice versa). Moreover, GCC can induce large-scale shifts in community composition, which may affect the vulnerability of communities to other stressors. Ecological modeling based on species traits (representing life-history traits, population vulnerability, sensitivity to toxicants, and sensitivity to climate change) can be a promising approach for predicting combined impacts of GCC and toxicants on populations and communities. Environ. Toxicol. Chem. 2013;32:49–61.

Thresholds, breakpoints, and nonlinearity in freshwaters as related to management

Abstract Nonlinear ecological responses to anthropogenic forcing are common, and in some cases, the ecosystem responds by assuming a new stable state. This article is an overview and serves as the introduction to several articles in this BRIDGES cluster that are directed toward managers interested in dealing with nonlinear responses in freshwaters, particularly streams. A threshold or breakpoint occurs where the system responds rapidly to a relatively small change in a driver. The existence of a threshold can signal a change in system configuration to an alternative stable state, although such a change does not occur with all thresholds. In general, a mechanistic understanding of ecological dynamics is required to predict thresholds, where they will occur, and if they are associated with the occurrence of alternative stable states. Thresholds are difficult to predict, although a variety of univariate methods has been used to indicate thresholds in ecological data. When we applied several methods to one type of response variable, the resulting threshold values varied 3-fold, indicating that more research on detection methods is necessary. Numerous case studies suggest that the threshold concept is important in all ecosystems. Managers should be aware that human actions might result in undesirable rapid changes and potentially an unwanted alternative stable state, and that recovery from that state might require far more resources and time than avoiding entering the state in the first place would have required. Given the difficulties in predicting thresholds and alternative states, the precautionary approach to ecosystem management is probably the most prudent.

SMALL-SCALE EXPERIMENTS SUPPORT CAUSAL RELATIONSHIPS BETWEEN METAL CONTAMINATION AND MACROINVERTEBRATE COMMUNITY RESPONSES

Routine biomonitoring studies that compare abundance of benthic macro- invertebrates upstream and downstream from contaminant discharges generally cannot be used to demonstrate causal relationships between stressors and biological responses. In this study I describe stream microcosm and field experiments designed to support results of a 12-year monitoring project in the metal-polluted Arkansas River, Colorado. Microcosm experiments established concentration-response relationships between heavy metals and several structural (abundance, richness) and functional (macroinvertebrate drift, community respiration) endpoints. EC10 values, the metal concentration that reduced abundance or richness by 10%, were generally lowest for mayflies and stoneflies, indicating greater metal sensitivity for these groups. Macroinvertebrate drift and community respiration showed highly significant concentration-response relationships with heavy metals and were gen- erally more sensitive than structural measures. Potential interactions among metals were investigated by comparing community-level responses to Zn alone, Zn+Cd, and Zn+Cu+Cd. Results showed that macroinvertebrate responses to a mixture of three metals were generally greater than responses to either Zn alone or Zn+Cd. Long-term monitoring in the Arkansas River (Colorado) before and after remediation of metal inputs provided correlative evidence that elevated heavy metal concentrations altered community compo- sition and reduced abundance of metal-sensitive organisms. However, these field data were not especially useful for estimating safe concentrations of heavy metals that would be protective of benthic communities. Microcosm and field experiments provided further sup- port for the hypothesis that metals caused alterations in benthic community structure and provided more precise estimates of safe metal concentrations.

RESPONSES OF DIATOM COMMUNITIES TO HEAVY METALS IN STREAMS: THE INFLUENCE OF LONGITUDINAL VARIATION

We investigated longitudinal variation (e.g., from upstream to downstream) in diatom community composition in an unpolluted stream (the Cache la Poudre River, Colorado, USA) and demonstrated how natural variation in community structure and mor- phological growth forms influence responses of diatoms in metal-polluted streams. Upstream communities in the Cache la Poudre River were physiognomically simple and dominated by small, adnate species (Achnanthes minutissima and Fragilaria vaucheriae), which de- creased in relative abundance downstream. Responses of diatom communities to Zn in six metal-polluted streams were influenced by elevation and other variables correlated with the streams longitudinal gradient (pH, conductivity, alkalinity). Although clear community responses were observed at sites where Zn concentration exceeded 200 VLg/L, effects of metals at moderately polluted sites were not significant. These field results were compared to responses of periphyton communities in experi- mental streams dosed with heavy metals. We hypothesized that communities collected from high elevation sites, which were dominated by early successional species (A. minutissima), would be more tolerant to metals than downstream communities. To test this hypothesis, diatom communities collected from a high elevation site (2340 m) and a low elevation site (1536 m) on the Cache la Poudre River were exposed to a mixture of Cd, Cu, and Zn in experimental streams. Small, adnate species (Achnanthes minutissima and Fragilaria vau- cheriae) were tolerant to metals and increased in abundance in treated streams. In contrast, late successional species, which were found only at the low elevation site (Diatoma vulgare and Melosira varians), were highly sensitive to metals and were eliminated from treated streams after 24 h. These results indicate that natural variation in diatom communities may complicate interpretation of routine biomonitoring studies. We suggest that it may be useful to study periphyton community responses to pollutants in relation to ecological character- istics and morphological growth forms. Conducting research within this framework may improve the predictive ability of periphyton models and provide a theoretical basis for understanding the relationships between community patterns and the evolutionary processes that determine responses to disturbance.

Integrating effects of contaminants across levels of biological organization: an overview

Effects of contaminants may occur at all levels oforganization, from molecular to ecosystem-levelresponses. While biochemical and physiologicalalterations in organisms may occur rapidly and areoften stressor-specific, the ecological relevance ofthese suborganismal indicators is uncertain.Alterations in populations and communities havegreater ecological relevance, but a firm mechanisticunderstanding of these responses is often lacking.Developing mechanistic linkages across levels ofbiological organization would greatly improve ourunderstanding of how organisms are affected bycontaminants in nature. The papers in this seriespresent several innovative approaches for integratingeffects of contaminants across levels of biologicalorganization. Authors were asked to describe theecological consequences of responses at lower levelsof organization (biochemical, physiological,individual) and to speculate on the underlyingmechanisms associated with population and communityalterations. The most consistent finding of the fivepapers in this series is that there is no singlespatiotemporal scale or level of biologicalorganization at which ecotoxicological investigationsshould be conducted.

Effects of Heavy Metals on a Macroinvertebrate Assemblage from a Rocky Mountain Stream in Experimental Microcosms

Natural assemblages of stream benthic macroinvertebrates were collected using artificial substrates from a Rocky Mountain stream and exposed for 10 d to a mixture of heavy metals (Cd, Cu, and Zn) in stream microcosms. Metal levels were 0, 1×, 5×, and 10× where × = 1.1, 12, and 110 μg/L Cd, Cu, and Zn, respectively. The 1× treatment was similar to chronic criteria values recommended by the US Environmental Protection Agency (EPA) for each metal and total metal levels measured in water at the Arkansas River, Colorado, a US EPA superfund site. Most ephemeropterans and plecopterans were sensitive to metals; however, some taxa within these groups were metal tolerant. Densities of Baetis tricaudatus (Ephemeroptera:Baetidae), Epeorus longimanus and Rhithrogena hageni (Ephemeroptera:Hepatageniidae), and Drunella grandis and D. doddsi (Ephemeroptera:Ephemerellidae) were reduced in the 1× treatment. The response of D. grandis to metals was size-dependent with small larvae being more sensitive than large ones (p = 0.02). Chironomids were generally tolerant to metals. These data show that a metal mixture was extremely toxic to stream macroinvertebrates from a Rocky Mountain stream. Our results were similar to field biomonitoring studies at the Arkansas River and Eagle River, Colorado, that examined the effects of metals on stream macroinvertebrate communities. We suggest that multispecies experiments using indigenous stream organisms be combined with field biomonitoring to rigorously define the biological effects of heavy metals on lotic systems.

METAL TOLERANCE AND PREDATOR–PREY INTERACTIONS IN BENTHIC MACROINVERTEBRATE STREAM COMMUNITIES

Predicting responses of benthic communities to contaminants requires an understanding of both direct and indirect effects. I examined the influence of previous exposure to heavy metals on metal tolerance and susceptibility of benthic communities to stonefly predation in experimental streams and field cages. Benthic communities obtained from a reference stream, the Cache la Poudre River (PR), and a metal-polluted stream, the Arkansas River (AR), in Colorado were exposed to a mixture of Cd, Cu, and Zn at ∼2× the U.S. EPA chronic criterion level (2.2 μg Cd/L, 24 μg Cu/L, and 220 μg Zn/L) for 10 d in stream microcosms. Effects of metals on survival were significantly greater on mayflies (Ephemeroptera) from the unpolluted PR than from the metal-polluted AR. Metal exposure also significantly increased drift of Rhithrogena hageni, the dominant mayfly in the unpolluted stream but had no effect on invertebrates from the AR. In a second experiment, communities from the two locations were exposed to predatory stoneflies (Claassenia sabulosa) in stream microcosms. Stonefly predation significantly reduced total macroinvertebrate abundance, number of taxa, and abundance of Baetis tricaudatus (Ephemeroptera) and R. hageni. Mayflies from the metal-polluted AR were also more susceptible to stonefly predation, but these results were probably influenced by differences in initial prey density. Results of caging experiments conducted at PR and AR field sites were consistent with results of laboratory experiments and showed that stonefly predation significantly reduced abundance of B. tricaudatus and R. hageni; however, effects of predation in the AR were relatively weak because of high prey immigration. Results of these experiments suggest that abiotic factors influence the outcome of species interactions in metal-polluted streams. Ecosystems disturbed by contaminants, particularly those polluted for relatively long periods of time, provide excellent opportunities to study these interactions.