Remarkable anoxia tolerance by stoneflies from a floodplain aquifer

Research output: Contribution to journalArticlepeer-review

14 Scopus citations

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.

Original languageEnglish
Article numbere03127
JournalEcology
Volume101
Issue number10
DOIs
StatePublished - Oct 1 2020

Funding

This work was funded by a National Science Foundation Dimensions of Biodiversity Grant #DOB-1639014 and approved under a Forest Service Special Use Permit. A. G. DelVecchia and J. A. Stanford were supported in part by NSF award DEB 1830178. M. Gamboa was supported by the Japanese Society for the Promotion of Science (JSPS) (Grant Number: 17H01666). We thank the Dalimata family for allowing us to conduct this research on their land and for helping with field support. Many lab and field crew members helped to collect the samples used in these experiments, including F. Breen, E. Keksi, E. Lee, M. McMillan, B. Prevelige, M. Ritter, W. Sigl, T. Schrock, and K. Whitmore. We thank FLBS Staff for support during lab experiments and P. Watson for early design of respiration experiments. This work was funded by a National Science Foundation Dimensions of Biodiversity Grant #DOB‐1639014 and approved under a Forest Service Special Use Permit. A. G. DelVecchia and J. A. Stanford were supported in part by NSF award DEB 1830178. M. Gamboa was supported by the Japanese Society for the Promotion of Science (JSPS) (Grant Number: 17H01666). We thank the Dalimata family for allowing us to conduct this research on their land and for helping with field support. Many lab and field crew members helped to collect the samples used in these experiments, including F. Breen, E. Keksi, E. Lee, M. McMillan, B. Prevelige, M. Ritter, W. Sigl, T. Schrock, and K. Whitmore. We thank FLBS Staff for support during lab experiments and P. Watson for early design of respiration experiments.

FundersFunder number
DEB 1830178, 1639014
Japan Society for the Promotion of Science17H01666

    Keywords

    • Plecoptera
    • anoxia tolerance
    • floodplain aquifer
    • floodplain biodiversity
    • mass-specific metabolic rates
    • methane-derived carbon

    Fingerprint

    Dive into the research topics of 'Remarkable anoxia tolerance by stoneflies from a floodplain aquifer'. Together they form a unique fingerprint.

    Cite this