Rock glaciers and related cold rocky landforms: Overlooked climate refugia for mountain biodiversity.

Mountains are global biodiversity hotspots where cold environments and their associated ecological communities are threatened by climate warming. Considerable research attention has been devoted to understanding the ecological effects of alpine glacier and snowfield recession. However, much less attention has been given to identifying climate refugia in mountain ecosystems where present-day environmental conditions will be maintained, at least in the near-term, as other habitats change. Around the world, montane communities of microbes, animals, and plants live on, adjacent to, and downstream of rock glaciers and related cold rocky landforms (CRL). These geomorphological features have been overlooked in the ecological literature despite being extremely common in mountain ranges worldwide with a propensity to support cold and stable habitats for aquatic and terrestrial biodiversity. CRLs are less responsive to atmospheric warming than alpine glaciers and snowfields due to the insulating nature and thermal inertia of their debris cover paired with their internal ventilation patterns. Thus, CRLs are likely to remain on the landscape after adjacent glaciers and snowfields have melted, thereby providing longer-term cold habitat for biodiversity living on and downstream of them. Here, we show that CRLs will likely act as key climate refugia for terrestrial and aquatic biodiversity in mountain ecosystems, offer guidelines for incorporating CRLs into conservation practices, and identify areas for future research.

Mountain stoneflies may tolerate warming streams: Evidence from organismal physiology and gene expression.

Rapid glacier recession is altering the physical conditions of headwater streams. Stream temperatures are predicted to rise and become increasingly variable, putting entire meltwater-associated biological communities at risk of extinction. Thus, there is a pressing need to understand how thermal stress affects mountain stream insects, particularly where glaciers are likely to vanish on contemporary timescales. In this study, we measured the critical thermal maximum (CTMAX ) of stonefly nymphs representing multiple species and a range of thermal regimes in the high Rocky Mountains, USA. We then collected RNA-sequencing data to assess how organismal thermal stress translated to the cellular level. Our focal species included the meltwater stonefly, Lednia tumana, which was recently listed under the U.S. Endangered Species Act due to climate-induced habitat loss. For all study species, critical thermal maxima (CTMAX  > 20°C) far exceeded the stream temperatures mountain stoneflies experience (<10°C). Moreover, while evidence for a cellular stress response was present, we also observed constitutive expression of genes encoding proteins known to underlie thermal stress (i.e., heat shock proteins) even at low temperatures that reflected natural conditions. We show that high-elevation aquatic insects may not be physiologically threatened by short-term exposure to warm temperatures and that longer-term physiological responses or biotic factors (e.g., competition) may better explain their extreme distributions.

Microbial assemblages reflect environmental heterogeneity in alpine streams.

Alpine streams are dynamic habitats harboring substantial biodiversity across small spatial extents. The diversity of alpine stream biota is largely reflective of environmental heterogeneity stemming from varying hydrological sources. Globally, alpine stream diversity is under threat as meltwater sources recede and stream conditions become increasingly homogeneous. Much attention has been devoted to macroinvertebrate diversity in alpine headwaters, yet to fully understand the breadth of climate change threats, a more thorough accounting of microbial diversity is needed. We characterized microbial diversity (specifically Bacteria and Archaea) of 13 streams in two disjunct Rocky Mountain subranges through 16S rRNA gene sequencing. Our study encompassed the spectrum of alpine stream sources (glaciers, snowfields, subterranean ice, and groundwater) and three microhabitats (ice, biofilms, and streamwater). We observed no difference in regional (γ) diversity between subranges but substantial differences in diversity among (ß) stream types and microhabitats. Within-stream (α) diversity was highest in groundwater-fed springs, lowest in glacier-fed streams, and positively correlated with water temperature for both streamwater and biofilm assemblages. We identified an underappreciated alpine stream type-the icy seep-that are fed by subterranean ice, exhibit cold temperatures (summer mean <2°C), moderate bed stability, and relatively high conductivity. Icy seeps will likely be important for combatting biodiversity losses as they contain similar microbial assemblages to streams fed by surface ice yet may be buffered against climate change by insulating debris cover. Our results show that the patterns of microbial diversity support an ominous trend for alpine stream biodiversity; as meltwater sources decline, stream communities will become more diverse locally, but regional diversity will be lost. Icy seeps, however, represent a source of optimism for the future of biodiversity in these imperiled ecosystems.

The influence of habitat heterogeneity and latitude on gamma diversity of the Nearctic Simuliidae, a ubiquitous group of stream-dwelling insects.

Among the most prominent, large-scale patterns of species richness are the increases in richness with decreasing latitude and with increasing habitat heterogeneity. Using the stream-dwelling larval and pupal stages of North American black flies (Diptera: Simuliidae), we address 3 broad questions about species richness: (i) Does a significant latitude-richness relationship exist? (ii) How does habitat heterogeneity influence gamma diversity? (iii) What is the sign (positive or negative) of the latitude-richness and the heterogeneity-richness relationships? We found no evidence that habitat heterogeneity influences gamma diversity. The estimated peak species richness for black flies in North America was at 50-53°N, which also corresponds with peak generic richness. All plesiomorphic, extant lineages of the Simuliidae in the Western Hemisphere are found in cool mountainous environments of North America, suggesting that peak richness at 50-53°N might be a signature of this phylogenetic pattern and a reflection of underlying historical processes.

Climate change and alpine stream biology: progress, challenges, and opportunities for the future.

In alpine regions worldwide, climate change is dramatically altering ecosystems and affecting biodiversity in many ways. For streams, receding alpine glaciers and snowfields, paired with altered precipitation regimes, are driving shifts in hydrology, species distributions, basal resources, and threatening the very existence of some habitats and biota. Alpine streams harbour substantial species and genetic diversity due to significant habitat insularity and environmental heterogeneity. Climate change is expected to affect alpine stream biodiversity across many levels of biological resolution from micro- to macroscopic organisms and genes to communities. Herein, we describe the current state of alpine stream biology from an organism-focused perspective. We begin by reviewing seven standard and emerging approaches that combine to form the current state of the discipline. We follow with a call for increased synthesis across existing approaches to improve understanding of how these imperiled ecosystems are responding to rapid environmental change. We then take a forward-looking viewpoint on how alpine stream biologists can make better use of existing data sets through temporal comparisons, integrate remote sensing and geographic information system (GIS) technologies, and apply genomic tools to refine knowledge of underlying evolutionary processes. We conclude with comments about the future of biodiversity conservation in alpine streams to confront the daunting challenge of mitigating the effects of rapid environmental change in these sentinel ecosystems.

Human effects on ecological connectivity in aquatic ecosystems: Integrating scientific approaches to support management and mitigation.

Understanding the drivers and implications of anthropogenic disturbance of ecological connectivity is a key concern for the conservation of biodiversity and ecosystem processes. Here, we review human activities that affect the movements and dispersal of aquatic organisms, including damming of rivers, river regulation, habitat loss and alteration, human-assisted dispersal of organisms and climate change. Using a series of case studies, we show that the insight needed to understand the nature and implications of connectivity, and to underpin conservation and management, is best achieved via data synthesis from multiple analytical approaches. We identify four key knowledge requirements for progressing our understanding of the effects of anthropogenic impacts on ecological connectivity: autecology; population structure; movement characteristics; and environmental tolerance/phenotypic plasticity. Structuring empirical research around these four broad data requirements, and using this information to parameterise appropriate models and develop management approaches, will allow for mitigation of the effects of anthropogenic disturbance on ecological connectivity in aquatic ecosystems.

Development and characterization of seven polymorphic microsatellite loci in Bembidion atrocaeruleum (Coleoptera: Carabidae).

We isolated seven polymorphic microsatellite loci from a ground beetle (Bembidion atrocaeruleum, Coleoptera, Carabidae (Stephens, 1826)) associated with naturally and regularly disturbed floodplain habitat in northwest Europe. Loci were tested on 157 individuals collected from five distinct habitat patches across two adjacent drainage basins in Wales, United Kingdom, to assess their potential for revealing population structure across a relatively short spatial extent. Alleles per locus ranged from 4 to 12. For a central representative population, expected heterozygosity ranged from 0.23 to 0.78 (mean: 0.63), and observed heterozygosity ranged from 0.16 to 0.94 (mean: 0.56). Analysis of molecular variance indicated significant structure among populations, even when one locus potentially containing null alleles was removed. These loci have the potential to aid the study of dispersal mechanisms of this important riparian species along and between river corridors, a recurring question in floodplain conservation studies. In addition, given the diversity of the Bembidion genus, they may have utility in the study of sister species.

Geomorphic and ecological disturbance and recovery from two small dams and their removal.

Dams are known to impact river channels and ecosystems, both during their lifetime and in their decommissioning. In this study, we applied a before-after-control-impact design associated with two small dam removals to investigate abiotic and biotic recovery trajectories from both the elimination of the press disturbance associated with the presence of dams and the introduction of a pulse disturbance associated with removal of dams. The two case studies represent different geomorphic and ecological conditions that we expected to represent low and high sensitivities to the pulse disturbance of dam removal: the 4 m tall, gravel-filled Brownsville Dam on the wadeable Calapooia River and the 12.5 m tall, sand and gravel-filled Savage Rapids Dam on the largely non-wadeable Rogue River. We evaluated both geomorphic and ecological responses annually for two years post removal, and asked if functional traits of the macroinvertebrate assemblages provided more persistent signals of ecological disturbance than taxonomically defined assemblages over the period of study. Results indicate that: 1) the presence of the dams constituted a strong ecological press disturbance to the near-downstream reaches on both rivers, despite the fact that both rivers passed unregulated flow and sediment during the high flow season; 2) ecological recovery from this press disturbance occurred within the year following the restoration action of dam removal, whereas signals of geomorphic disturbance from the pulse of released sediment persisted two years post-removal, and 3) the strength of the press disturbance and the rapid ecological recovery were detected regardless of whether recovery was assessed by taxonomic or functional assemblages and for both case studies, in spite of their different geomorphic settings.

Demographic stability metrics for conservation prioritization of isolated populations.

Systems of geographically isolated habitat patches house species that occur naturally as small, disjunct populations. Many of these species are of conservation concern, particularly under the interacting influences of isolation and rapid global change. One potential conservation strategy is to prioritize the populations most likely to persist through change and act as sources for future recolonization of less stable localities. We propose an approach to classify long-term population stability (and, presumably, future persistence potential) with composite demographic metrics derived from standard population-genetic data. Stability metrics can be related to simple habitat measures for a straightforward method of classifying localities to inform conservation management. We tested these ideas in a system of isolated desert headwater streams with mitochondrial sequence data from 16 populations of a flightless aquatic insect. Populations exhibited a wide range of stability scores, which were significantly predicted by dry-season aquatic habitat size. This preliminary test suggests strong potential for our proposed method of classifying isolated populations according to persistence potential. The approach is complementary to existing methods for prioritizing local habitats according to diversity patterns and should be tested further in other systems and with additional loci to inform composite demographic stability scores.

Evolution of aquatic insect behaviours across a gradient of disturbance predictability.

Natural disturbance regimes--cycles of fire, flood, drought or other events--range from highly predictable (disturbances occur regularly in time or in concert with a proximate cue) to highly unpredictable. While theory predicts how populations should evolve under different degrees of disturbance predictability, there is little empirical evidence of how this occurs in nature. Here, we demonstrate local adaptation in populations of an aquatic insect occupying sites along a natural gradient of disturbance predictability, where predictability was defined as the ability of a proximate cue (rainfall) to signal a disturbance (flash flood). In controlled behavioural experiments, populations from predictable environments responded to rainfall events by quickly exiting the water and moving sufficiently far from the stream to escape flash floods. By contrast, populations from less predictable environments had longer response times and lower response rates, reflecting the uncertainty inherent to these environments. Analysis with signal detection theory showed that for 13 out of 15 populations, observed response times were an optimal compromise between the competing risks of abandoning versus remaining in the stream, mediated by the rainfall-flood correlation of the local environment. Our study provides the first demonstration that populations can evolve in response to differences in disturbance predictability, and provides evidence that populations can adapt to among-stream differences in flow regime.

Spatial population genetic structure and limited dispersal in a Rocky Mountain alpine stream insect.

Using the mitochondrial cytochrome oxidase I (COI) gene, we assessed the phylogeographic structure of Prosimulium neomacropyga, a black fly (Simuliidae) whose distribution in the US Southern Rockies ecoregion is limited to alpine tundra streams. Given high habitat specificity, lack of hydrological connection between streams, and a terrestrial environment restrictive to insect flight, we hypothesized limited gene flow. A spatially nested sampling design showed that grouping populations according to high-elevation 'islands' of alpine tundra (which typically include headwater streams of > 1 watershed) explained a significant proportion of genetic variation while grouping streams according to major watershed (across islands) did not. Nested clade analysis and isolation-by-distance (IBD) relationships further implicated limited ongoing gene flow within but not among the isolated alpine islands. IBD was strong among five streams within an individual island using each of four alternative models of pairwise landscape connectivity for flying insects. Results of all landscape models were positively correlated, suggesting that straight-line distance is an acceptable surrogate for presumably more biologically meaningful connectivity measures in this system. IBD was significantly weaker across the entire study area, comprised of three separate islands. Overall, population structure was significant with F(ST) = 0.38, suggesting limited dispersal across a small spatial extent.

Geographic variation in patterns of nestedness among local stream fish assemblages in Virginia.

Nestedness of faunal assemblages is a multi-scale phenomenon, potentially influenced by a variety of factors. Prior small-scale studies have found freshwater fish species assemblages to be nested along stream courses as a result of either selective colonization or extinction. However, within-stream gradients in temperature and other factors are correlated with the distributions of many fish species and may also contribute to nestedness. At a regional level, strongly nested patterns would require a consistent set of structuring mechanisms across streams, and correlation among species' tolerances of the environmental factors that influence distribution. Thus, nestedness should be negatively associated with the spatial extent of the region analyzed and positively associated with elevational gradients (a correlate of temperature and other environmental factors). We examined these relationships for the freshwater fishes of Virginia. Regions were defined within a spatial hierarchy and included whole river drainages, portions of drainages within physiographic provinces, and smaller subdrainages. In most cases, nestedness was significantly stronger in regions of smaller spatial extent and in regions characterized by greater topographic relief. Analysis of hydrologic variability and patterns of faunal turnover provided no evidence that inter-annual colonization/extinction dynamics contributed to elevational differences in nestedness. These results suggest that, at regional scales, nestedness is influenced by interactions between biotic and abiotic factors, and that the strongest nestedness is likely to occur where a small number of organizational processes predominate, i.show $132#e., over small spatial extents and regions exhibiting strong environmental gradients.