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ABSTRACT Aquatic insects cope with hypoxia and anoxia using a variety of behavioral and physiological responses. Most stoneflies (Plecoptera) occur in highly oxygenated surface waters, but some species live underground in alluvial aquifers containing heterogeneous oxygen concentrations. Aquifer stoneflies appear to be supported by methane-derived food resources, which they may exploit using anoxia-resistant behaviors. We documented dissolved oxygen dynamics and collected stoneflies over 5 years in floodplain wells of the Flathead River, Montana. Hypoxia regularly occurred in two wells, and nymphs of Paraperla frontalis were collected during hypoxic periods. We measured mass-specific metabolic rates (MSMRs) at different oxygen concentrations (12, 8, 6, 4, 2, 0.5 mg l −1 , and during recovery) for 111 stonefly nymphs to determine whether aquifer and benthic taxa differed in hypoxia tolerance. Metabolic rates of aquifer taxa were similar across oxygen concentrations spanning 2 to 12 mg l −1 ( P >0.437), but the MSMRs of benthic taxa dropped significantly with declining oxygen ( P <0.0001; 2.9-times lower at 2 vs. 12 mg l −1 ). Aquifer taxa tolerated short-term repeated exposure to extreme hypoxia surprisingly well (100% survival), but repeated longer-term (>12 h) exposures resulted in lower survival (38–91%) and lower MSMRs during recovery. Our work suggests that aquifer stoneflies have evolved a remarkable set of behavioral and physiological adaptations that allow them to exploit the unique food resources available in hypoxic zones. These adaptations help to explain how large-bodied consumers might thrive in the underground aquifers of diverse and productive river floodplains. 

Abstract Little is known about the life histories, genetic structure and population connectivity of shallow groundwater organisms. We used next-generation sequencing (RAD-seq) to analyse population genomic structure in two aquifer species: Paraperla frontalis (Banks, 1902), a stonefly with groundwater larvae and aerial (winged) adults; and Stygobromus sp., a groundwater-obligate amphipod. We found similar genetic differentiation in each species between floodplains separated by ~70 river km in the Flathead River basin of north-west Montana, USA. Given that Stygobromus lacks the above-ground life stage of P. frontalis, our findings suggest that connectivity and the magnitude of genetic structure cannot be definitively assumed from life history differences. 

Alluvial aquifers are key components of river floodplains and biodiversity worldwide, but they contain extreme environmental conditions and have limited sources of carbon for sustaining food webs. Despite this, they support abundant populations of aquifer stoneflies that have large proportions of their biomass carbon derived from methane. Methane is typically produced in freshwater ecosystems in anoxic conditions, while stoneflies (Order: Plecoptera) are thought to require highly oxygenated water. The potential importance of methane‐derived food resources raises the possibility that stonefly consumers have evolved anoxia‐resistant behaviors and physiologies. Here we tested the anoxic and hypoxic responses of 2,445 stonefly individuals in three aquifer species and nine benthic species. We conducted experimental trials in which we reduced oxygen levels, documented locomotor activity, and measured survival rates. Compared to surface‐dwelling benthic relatives, stoneflies from the alluvial aquifer on the Flathead River (Montana) performed better in hypoxic and anoxic conditions. Aquifer species sustained the ability to walk after 4–76 h of anoxia vs. 1 h for benthic species and survived on average three times longer than their benthic counterparts. Aquifer stoneflies also sustained aerobic respiration down to much lower levels of ambient oxygen. We show that aquifer taxa have gene sequences for hemocyanin, an oxygen transport respiratory protein, representing a possible mechanism for surviving low oxygen. This remarkable ability to perform well in low‐oxygen conditions is unique within the entire order of stoneflies (Plecoptera) and uncommon in other freshwater invertebrates. These results show that aquifer stoneflies can exploit rich carbon resources available in anoxic zones, which may explain their extraordinarily high abundance in gravel‐bed floodplain aquifers. These stoneflies are part of a novel food web contributing biodiversity to river floodplains.

 

Understanding how environmental variation influences population genetic structure is important for conservation management because it can reveal how human stressors influence population connectivity, genetic diversity and persistence. We used riverscape genetics modelling to assess whether climatic and habitat variables were related to neutral and adaptive patterns of genetic differentiation (population‐specific and pairwiseF_ST) within five metapopulations (79 populations, 4583 individuals) of steelhead trout (Oncorhynchus mykiss) in the Columbia River Basin,USA. Using 151 putatively neutral and 29 candidate adaptiveSNPloci, we found that climate‐related variables (winter precipitation, summer maximum temperature, winter highest 5% flow events and summer mean flow) best explained neutral and adaptive patterns of genetic differentiation within metapopulations, suggesting that climatic variation likely influences both demography (neutral variation) and local adaptation (adaptive variation). However, we did not observe consistent relationships between climate variables andF_STacross all metapopulations, underscoring the need for replication when extrapolating results from one scale to another (e.g. basin‐wide to the metapopulation scale). Sensitivity analysis (leave‐one‐population‐out) revealed consistent relationships between climate variables andF_STwithinthree metapopulations; however, these patterns were not consistent in two metapopulations likely due to small sample sizes (N = 10). These results provide correlative evidence that climatic variation has shaped the genetic structure of steelhead populations and highlight the need for replication and sensitivity analyses in land and riverscape genetics.