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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. 

Abstract 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.