Abstract
The saturated interstices below and adjacent to the riverbed (i.e., the hyporheic zone) can be a refuge for biota during low flows, flow cessation and river drying. Prior to complete drying, organisms are constrained by abiotic and biotic factors (e.g., water temperature, competition) and may respond through vertical migration into the hyporheic zone. However, it remains unclear when temperature and competition become harsh enough to trigger migration. Furthermore, potential consequences of using the hyporheic zone, which is often food-limited, on the survival, effects on ecosystem function and physiology of organisms are unknown. We tested the hypotheses that (1) Gammarus pulex, a widespread detritivore, migrates into the hyporheic zone to avoid increasing surface water temperature and intraspecific competition and (2) that these factors would reduce their survival, leaf mass consumption and energy stores. Using 36 mesocosms, three temperature (15, 20, 25 °C) and species density levels (low, medium, high) were manipulated in a factorial design over 15 days. Increasing temperature to 25 °C and a threefold increase in density both caused G. pulex to vertically migrate, and the interaction of these factors was additive, rather than antagonistic or synergistic. Importantly, survival, leaf consumption and glycogen content were reduced in high temperature and density treatments, suggesting tradeoffs between tolerating harsh surface conditions and limitations of inhabiting the hyporheic zone. Identifying that the hyporheic zone is used by G. pulex to avoid high water temperature and intraspecific competition is a key finding considering the global-scale increases in temperature and flow intermittence.
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Acuña V, Muñoz I, Giorgi A, Omella M, Sabater F, Sabater S (2005) Drought and postdrought recovery cycles in an intermittent Mediterranean stream: structural and functional aspects. J N Am Benthol Soc 24:919–933. doi:10.1899/04-078.1
Boersma KS, Bogan MT, Henrichs BA, Lytle DA (2014) Top predator removals have consistent effects on large species despite high environmental variability. Oikos 123:807–816. doi:10.1111/oik.00925
Boulton AJ (1989) Over-summering refuges of aquatic macroinvertebrates in two intermittent streams in central Victoria Australia. Trans R Soc S Aust 113:23–34
Burnside WR, Erhardt EB, Hammond ST, Brown JH (2014) Rates of biotic interactions scale predictably with temperature despite variation. Oikos 123:1449–1456. doi:10.1111/oik.01199
Burrell GP, Ledger ME (2003) Growth of a stream-dwelling caddisfly (Olinga feredayi: Conoesucidae) on surface and hyporheic food resources. J N Am Benthol Soc 22:92–104. doi:10.2307/1467980
Capderrey C, Datry T, Foulquier A, Claret C, Malard F (2013) Invertebrate distribution across nested geomorphic features in braided-river landscapes. Freshw Sci 32:1188–1204. doi:10.1899/12-188.1
Constantz J, Thomas CL (1997) Stream bed temperature profiles as indicators of percolation characteristics beneath arroyos in the middle Rio Grande Basin, USA. Hydrol Process 11:1621–1634. doi:10.1002/(SICI)1099-1085(19971015)11:12<1621:AID-HYP493>3.0.CO;2-X
Corti R, Datry T, Drummond L, Larned ST (2011) Natural variation in immersion and emersion affects breakdown and invertebrate colonization of leaf litter in a temporary river. Aquat Sci 73:537–550. doi:10.1007/s00027-011-0216-5
Covich AP, Crowl TA, Scatena FN (2003) Effects of extreme low flows on freshwater shrimps in a perennial tropical stream. Freshw Biol 48:119–1206. doi:10.1046/j.1365-2427.2003.01093.x
Danger M, Cornut J, Elger A, Chauvet E (2012) Effects of burial on leaf litter quality, microbial conditioning and palatability to three shredder taxa. Freshw Biol 57:1017–1030. doi:10.1111/j.1365-2427.2012.02762.x
Dangles O, Malmqvist B (2004) Species richness–decomposition relationships depend on species dominance. Ecol Lett 7:395–402. doi:10.1111/j.1461-0248.2004.00591.x
Datry T, Corti R, Claret C, Philippe M (2011) Flow intermittence controls leaf litter breakdown in a French temporary alluvial river: the “drying memory”. Aquat Sci 73:471–483. doi:10.1007/s00027-011-0193-8
Datry T, Larned ST, Tockner K (2014) Intermittent rivers: a challenge for freshwater ecology. Bioscience. doi:10.1093/biosci/bit1027
Descloux S, Datry T, Marmonier P (2013) Benthic and hyporheic invertebrate assemblages along a gradient of increasing streambed colmation by fine sediment. Aquat Sci 75:493–507. doi:10.1007/s00027-013-0295-6
DiStefano RJ, Magoulick DD, Imhoff EM, Larson ER (2009) Imperiled crayfishes use hyporheic zone during seasonal drying of an intermittent stream. J N Am Benthol Soc 28:142–152. doi:10.1899/08-072.1
Dole-Olivier MJ, Marmonier P, Beffy JL (1997) Response of invertebrates to lotic disturbance: is the hyporheic zone a patchy refugium? Freshw Biol 37:257–276. doi:10.1046/j.1365-2427.1997.00140.x
Elliott JM (2005) Day–night changes in the spatial distribution and habitat preferences of freshwater shrimps, Gammarus pulex, in a stony stream. Freshw Biol 50:552–566. doi:10.1111/j.1365-2427.2005.01345.x
Fairchild MP, Holomuzki JR (2005) Multiple predator effects on microdistributions, survival, and drift of stream hydropsychid caddisflies. J N Am Benthol Soc 24:101–112. doi:10.1899/0887-3593(2005)024<0101:MPEOMS>2.0.CO;2
Ferreira V, Canhoto C (2015) Future increase in temperature may stimulate litter decomposition in temperate mountain streams: evidence from a stream manipulation experiment. Freshw Biol. doi:10.1111/fwb.12539
Findlay S (1995) Importance of surface–subsurface exchange in stream ecosystems: the hyporheic zone. Limnol Oceanogr 40:159–164. doi:10.4319/lo.1995.40.1.0159
Foucreau N, Piscart C, Puijalon S, Hervant F (2013) Effect of climate-related change in vegetation on leaf litter consumption and energy storage by Gammarus pulex from continental or Mediterranean populations. PLoS One 8:e77242. doi:10.1371/journal.pone.0077242
Foucreau N, Cottin D, Piscart C, Hervant F (2014) Physiological and metabolic responses to rising temperature in Gammarus pulex (Crustacea) populations living under continental or Mediterranean climates. Comp Biochem Physiol A Mol Integr Physiol 168:69–75. doi:10.1016/j.cbpa.2013.11.006
Heino J, Melo AS, Siqueira T, Soininen J, Valanko S, Bini LM (2015) Metacommunity organisation, spatial extent and dispersal in aquatic systems: patterns, processes and prospects. Freshw Biol 60:845–869. doi:10.1111/fwb.12533
Hervant F, Mathieu J, Barré H, Simon K, Pinon C (1997) Comparative study on the behavioral, ventilatory, and respiratory responses of hypogean and epigean crustaceans to long-term starvation and subsequent feeding. Comp Biochem Physiol A Physiol 118:1277–1283
Hervant F, Mathieu J, Barré H (1999) Comparative study on the metabolic responses of subterranean and surface-dwelling amphipods to long-term starvation and subsequent refeeding. J Exp Biol 202(24):3587–3595
Holomuzki JR, Biggs BJ (2007) Physical microhabitat effects on 3-dimensional spatial variability of the hydrobiid snail, Potamopyrgus antipodarum. N Z J Mar Freshw Res 41:357–367. doi:10.1080/00288330709509925
Jaeger KL, Olden JD, Pelland NA (2014) Climate change poised to threaten hydrologic connectivity and endemic fishes in dryland streams. Proc Natl Acad Sci. doi:10.1073/pnas.1320890111
James AB, Dewson ZS, Death RG (2008) Do stream macroinvertebrates use instream refugia in response to severe short-term flow reduction in New Zealand streams? Freshw Biol 53:1316–1334. doi:10.1111/j.1365-2427.2008.01969.x
Lake PS (2003) Ecological effects of perturbation by drought in flowing waters. Freshw Biol 48:1161–1172. doi:10.1046/j.1365-2427.2003.01086.x
MacNeil C, Dick JTA, Elwood RW (1997) The trophic ecology of freshwater Gammarus spp. (Crustacea: Amphipoda): problems and perspectives concerning the functional feeding group concept. Biol Rev 72:349–364. doi:10.1111/j.1469-185X.1997.tb00017.x
Mas-Martí E, Muñoz I, Oliva F, Canhoto C (2015) Effects of increased water temperature on leaf litter quality and detritivore performance: a whole-reach manipulative experiment. Freshw Biol 60:184–197. doi:10.1111/fwb.12485
Mathers KL, Millett J, Robertson AL, Stubbington R, Wood PJ (2014) Faunal response to benthic and hyporheic sedimentation varies with direction of vertical hydrological exchange. Freshw Biol 59:2278–2289. doi:10.1111/fwb.12430
Mathews C (1967) The energy budget and nitrogen turnover of a population of Gammarus pulex in a small woodland stream. J Anim Ecol 36:62–69
McGrath KE, Peeters E, Beijer J, Scheffer M (2007) Habitat-mediated cannibalism and microhabitat restriction in the stream invertebrate Gammarus pulex. Hydrobiologia 589:155–164. doi:10.1007/s10750-007-0731-5
Mouthon J, Daufresne M (2006) Effects of the 2003 heatwave and climatic warming on mollusc communities of the Saône: a large lowland river and of its two main tributaries (France). Glob Change Biol 12:441–449. doi:10.1111/j.1365-2486.2006.01095.x
Navel S, Mermillod-Blondin F, Montuelle B, Chauvet E, Simon L, Piscart C, Marmonier P (2010) Interactions between fauna and sediment control the breakdown of plant matter in river sediments. Freshw Biol 55:753–766. doi:10.1111/j.1365-2427.2009.02315.x
Olsen DA, Townsend CR (2003) Hyporheic community composition in a gravel-bed stream: influence of vertical hydrological exchange, sediment structure and physicochemistry. Freshw Biol 48:1363–1378. doi:10.1046/j.1365-2427.2003.01097.x
Ormerod SJ, Dobson M, Hildrew AG, Townsend CR (2010) Multiple stressors in freshwater ecosystems. Freshw Biol 55:1–4. doi:10.1111/j.1365-2427.2009.02395.x
Palmer MA, Bely AE, Berg KE (1992) Response of invertebrates to lotic disturbance: a test of the hyporheic refuge hypothesis. Oecologia 89:182–194. doi:10.1007/BF00317217
Postel SL (2000) Entering an era of water scarcity: the challenges ahead. Ecol Appl 10:941–948. doi:10.1890/1051-0761(2000)010[0941:EAEOWS]2.0.CO;2
Salin K, Voituron Y, Mourin J, Hervant F (2010) Cave colonization without fasting capacities: an example with the fish Astyanax fasciatus mexicanus. Comp Biochem Physiol A Mol Integr Physiol 156:451–457. doi:10.1016/j.cbpa.2010.03.030
Schmid PE, Schmid-Araya JM (1997) Predation on meiobenthic assemblages: resource use of a tanypod guild (Chironomidae, Diptera) in a gravel stream. Freshw Biol 38:67–91. doi:10.1046/j.1365-2427.1997.00197.x
Stanley EH, Buschman DL, Boulton AJ, Grimm NB, Fisher SG (1994) Invertebrate resistance and resilience to intermittency in a desert stream. Am Midl Nat 131:288–300. doi:10.2307/2426255
Stewart B, Close P, Cook P, Davies P (2013a) Upper thermal tolerances of key taxonomic groups of stream invertebrates. Hydrobiologia 718:131–140. doi:10.1007/s10750-013-1611-9
Stewart RI et al (2013b) Mesocosm experiments as a tool for ecological climate-change research. Adv Ecol Res 48:71–181. doi:10.1016/B978-0-12-417199-2.00002-1
Stubbington R (2012) The hyporheic zone as an invertebrate refuge: a review of variability in space, time, taxa and behaviour. Mar Freshw Res 63:293–311. doi:10.1071/MF11196
Stubbington R, Wood PJ, Reid I, Gunn J (2011) Benthic and hyporheic invertebrate community responses to seasonal flow recession in a groundwater-dominated stream. Ecohydrology 4:500–511. doi:10.1002/eco.168
Sutcliffe DW, Carrick TR, Willoughby LG (1981) Effects of diet, body size, age and temperature on growth rates in the amphipod Gammarus pulex. Freshw Biol 11:183–214. doi:10.1111/j.1365-2427.1981.tb01252.x
Vadher AN, Stubbington R, Wood PJ (2015) Fine sediment reduces vertical migrations of Gammarus pulex (Crustacea: Amphipoda) in response to surface water loss. Hydrobiologia 753:61–71. doi:10.1007/s10750-015-2193-5
van Vliet MTH, Franssen WHP, Yearsley JR, Ludwig F, Haddeland I, Lettenmaier DP, Kabat P (2013) Global river discharge and water temperature under climate change. Glob Environ Change 23:450–464. doi:10.1016/j.gloenvcha.2012.11.002
Vander Vorste R, Malard F, Datry T (2015) Is drift the primary process promoting the resilience of river invertebrate communities? A manipulative field experiment in an intermittent alluvial river. Freshw Biol. doi:10.1111/fwb.12658
Welton JS (1979) Life-history and production of the amphipod Gammarus pulex in a Dorset chalk stream. Freshw Biol 9:263–275. doi:10.1111/j.1365-2427.1979.tb01508.x
White DS (1993) Perspectives on defining and delineating hyporheic zones. J N Am Benthol Soc 12:61–69. doi:10.2307/1467686
Williams DD, Moore KA (1985) The role of semiochemicals in benthic community relationships of the lotic amphipod Gammarus pseudolimnaeus: a laboratory analysis. Oikos 44:280–286. doi:10.2307/3544701
Wood PJ, Boulton AJ, Little S, Stubbington R (2010) Is the hyporheic zone a refugium for aquatic macroinvertebrates during severe low flow conditions? Fundam Appl Limnol 176:377–390. doi:10.1127/1863-9135/2010/0176-0377
Wooster DE, DeBano SJ, Madsen A (2011) Predators are more important than conspecifics and water temperature in influencing the microdistribution and behavior of a detritivorous stonefly. Fundam Appl Limnol 179:215–223. doi:10.1127/1863-9135/2011/0179-0215
Acknowledgments
This project was funded by the Rhône-Méditerranée-Corse Water Agency through the “Invertebrate community resistance and resilience in intermittent rivers” project, with support for RV from IRSTEA. Thoughtful discussions with Florian Malard were influential to the study design. We thank Maxence Forcellini, Bertrand Launay and Guillaume Le Goff for helping collect and count G. pulex in the field and laboratory. Stuart Findlay, Andrew Boulton, Paul Wood and two anonymous reviewers provided excellent feedback and suggestions to improve this manuscript.
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Vander Vorste, R., Mermillod-Blondin, F., Hervant, F. et al. Gammarus pulex (Crustacea: Amphipoda) avoids increasing water temperature and intraspecific competition through vertical migration into the hyporheic zone: a mesocosm experiment. Aquat Sci 79, 45–55 (2017). https://doi.org/10.1007/s00027-016-0478-z
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DOI: https://doi.org/10.1007/s00027-016-0478-z