Step-patterned survivorship curves: Mortality and loss of equilibrium responses to high temperature and food restriction in juvenile rainbow trout (Oncorhynchus mykiss)

Gosselin, Jennifer L.; Anderson, James J.

doi:10.1371/journal.pone.0233699

Title: Step-patterned survivorship curves: Mortality and loss of equilibrium responses to high temperature and food restriction in juvenile rainbow trout (Oncorhynchus mykiss)

Journal Article · Fri May 29 00:00:00 UTC 2020 · PLoS ONE

DOI: https://doi.org/10.1371/journal.pone.0233699 · OSTI ID:1903798

^[1]; Anderson, James J. ^[2]

University of Washington, Seattle, WA (United States); OSTI
University of Washington, Seattle, WA (United States)

While survivorship curves typically exhibit smooth declines over time, step-patterned curves can occur with multiple stressors within a life stage. To explore this process, we examined the effects of heat (24°C) and food restriction on juvenile rainbow trout (Oncorhynchus mykiss Walbaum) in challenge experiments. We observed step-patterned survivorship curves determined by mortality and loss of equilibrium (LOE) endpoints. To examine the cause of heterogeneity in the stress responses from early to late mortality and LOE, we measured indices of energetic reserves. The step transition in the survivorship curves, the peak mortality rates, and start of when individuals reached a critical energetic threshold (14% dry mass; 4.0 kJ∙g^-1 energy) all occurred at around days 10–15 of the challenge. The coherence in these temporal patterns suggest heterogeneity in the cohort stress responses, in which an early subgroup died from heat stress and a late subgroup died from starvation. Thus, their endpoint sensitivities resulted in step-patterned survivorship curves. We discuss the implications of the study for understanding effects of multiple stressors on population heterogeneity and note the possible significance of stress response selection under climate change in which heat stress and food limitations occur in concert.

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Research Organization:: University of Washington, Seattle, WA (United States)

Sponsoring Organization:: Marsha Landolt and Robert Busch Endowed Fund; USDOE USDOE Bonneville Power Administration

OSTI ID:: 1903798

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 5 Vol. 15; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

References (73)

Cellular response to oxidative stress: Signaling for suicide and survival Martindale, Jennifer L.; Holbrook, Nikki J. Journal of Cellular Physiology, Vol. 192, Issue 1 https://doi.org/10.1002/jcp.10119	journal	June 2002
Energy Depletion and Stress Levels in Sockeye Salmon Migrating at the Northern Edge of their Distribution Carey, Michael P.; Keith, Kevin D.; Schelske, Merlyn Transactions of the American Fisheries Society, Vol. 148, Issue 4 https://doi.org/10.1002/tafs.10172	journal	June 2019
Effects of cold and heat on behavior and cerebellar function in goldfish Friedlander, M. J.; Kotchabhakdi, N.; Prosser, C. L. Journal of Comparative Physiology ? A, Vol. 112, Issue 1 https://doi.org/10.1007/BF00612674	journal	January 1976
When warming hits harder: survival, cellular stress and thermal limits of Sparus aurata larvae under global change Madeira, Diana; Costa, Pedro M.; Vinagre, Catarina Marine Biology, Vol. 163, Issue 4 https://doi.org/10.1007/s00227-016-2856-4	journal	March 2016
Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals Fitt, William; Brown, Barbara; Warner, Mark Coral Reefs, Vol. 20, Issue 1 https://doi.org/10.1007/s003380100146	journal	August 2001
Resource competition induces heterogeneity and can increase cohort survivorship: selection-event duration matters Gosselin, Jennifer L.; Anderson, James J. Oecologia, Vol. 173, Issue 4 https://doi.org/10.1007/s00442-013-2736-2	journal	August 2013
Climate change impacts on streamflow extremes and summertime stream temperature and their possible consequences for freshwater salmon habitat in Washington State Mantua, Nathan; Tohver, Ingrid; Hamlet, Alan Climatic Change, Vol. 102, Issue 1-2 https://doi.org/10.1007/s10584-010-9845-2	journal	April 2010
Heat Shock Protein 70 kDa Molecular Biology, Biochemistry, and Physiology Kiang, J. Pharmacology & Therapeutics, Vol. 80, Issue 2 https://doi.org/10.1016/S0163-7258(98)00028-X	journal	November 1998
Habitat requirements of Atlantic salmon and brown trout in rivers and streams Armstrong, J. D.; Kemp, P. S.; Kennedy, G. J. A. Fisheries Research, Vol. 62, Issue 2 https://doi.org/10.1016/S0165-7836(02)00160-1	journal	May 2003
A parameter estimation routine for the vitality-based survival model Salinger, David H.; Anderson, James J.; Hamel, Owen S. Ecological Modelling, Vol. 166, Issue 3 https://doi.org/10.1016/S0304-3800(03)00162-5	journal	August 2003
Heat shock protein genes and their functional significance in fish Basu, N.; Todgham, A. E.; Ackerman, P. A. Gene, Vol. 295, Issue 2 https://doi.org/10.1016/S0378-1119(02)00687-X	journal	August 2002
Future frequencies of extreme weather events in the National Wildlife Refuges of the conterminous U.S. Martinuzzi, Sebastián; Allstadt, Andrew J.; Bateman, Brooke L. Biological Conservation, Vol. 201 https://doi.org/10.1016/j.biocon.2016.07.007	journal	September 2016
Physiology of temperature regulation: Comparative aspects Bicego, Kênia C.; Barros, Renata C. H.; Branco, Luiz G. S. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, Vol. 147, Issue 3 https://doi.org/10.1016/j.cbpa.2006.06.032	journal	July 2007
Starvation physiology: Reviewing the different strategies animals use to survive a common challenge McCue, Marshall D. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, Vol. 156, Issue 1 https://doi.org/10.1016/j.cbpa.2010.01.002	journal	May 2010
Are fish in hot water? Effects of warming on oxidative stress metabolism in the commercial species Sparus aurata Madeira, Diana; Vinagre, Catarina; Diniz, Mário S. Ecological Indicators, Vol. 63 https://doi.org/10.1016/j.ecolind.2015.12.008	journal	April 2016
Ocean warming alters cellular metabolism and induces mortality in fish early life stages: A proteomic approach Madeira, D.; Araújo, J. E.; Vitorino, R. Environmental Research, Vol. 148 https://doi.org/10.1016/j.envres.2016.03.030	journal	July 2016
Visualizing hidden heterogeneity in isogenic populations of C. elegans Wu, D.; Rea, S.; Yashin, A. Experimental Gerontology, Vol. 41, Issue 3 https://doi.org/10.1016/j.exger.2006.01.003	journal	March 2006
A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests Allen, Craig D.; Macalady, Alison K.; Chenchouni, Haroun Forest Ecology and Management, Vol. 259, Issue 4 https://doi.org/10.1016/j.foreco.2009.09.001	journal	February 2010
Prior heat accumulation reduces survival during subsequent experimental heat waves Siegle, Matthew R.; Taylor, Eric B.; O'Connor, Mary I. Journal of Experimental Marine Biology and Ecology, Vol. 501 https://doi.org/10.1016/j.jembe.2018.01.012	journal	April 2018
The rise and fall of the “marine heat wave” off Western Australia during the summer of 2010/2011 Pearce, Alan F.; Feng, Ming Journal of Marine Systems, Vol. 111-112 https://doi.org/10.1016/j.jmarsys.2012.10.009	journal	February 2013
When and how should intraspecific variability be considered in trait-based plant ecology? Albert, Cécile H.; Grassein, Fabrice; Schurr, Frank M. Perspectives in Plant Ecology, Evolution and Systematics, Vol. 13, Issue 3 https://doi.org/10.1016/j.ppees.2011.04.003	journal	September 2011
The vitality model: A way to understand population survival and demographic heterogeneity Li, Ting; Anderson, James J. Theoretical Population Biology, Vol. 76, Issue 2 https://doi.org/10.1016/j.tpb.2009.05.004	journal	September 2009
A thermosensory pathway that controls body temperature Nakamura, Kazuhiro; Morrison, Shaun F. Nature Neuroscience, Vol. 11, Issue 1 https://doi.org/10.1038/nn2027	journal	December 2007
Functional significance of isoenzymes in thermal acclimatization. Acetylcholinesterase from trout brain Baldwin, John; Hochachka, P. W. Biochemical Journal, Vol. 116, Issue 5 https://doi.org/10.1042/bj1160883	journal	March 1970
Combining Migration History, River Conditions, and Fish Condition to Examine Cross-Life-Stage Effects on Marine Survival in Chinook Salmon Gosselin, J. L.; Anderson, J. J. Transactions of the American Fisheries Society, Vol. 146, Issue 3 https://doi.org/10.1080/00028487.2017.1281166	journal	March 2017
Research in Thermal Biology: Burning Questions for Coldwater Stream Fishes McCullough, Dale A.; Bartholow, John M.; Jager, Henriëtte I. Reviews in Fisheries Science, Vol. 17, Issue 1 https://doi.org/10.1080/10641260802590152	journal	January 2009
The Ecology of Individuals: Incidence and Implications of Individual Specialization Bolnick, Daniel I.; Svanbäck, Richard; Fordyce, James A. The American Naturalist, Vol. 161, Issue 1 https://doi.org/10.1086/343878	journal	January 2003
Some Principles in the Thermal Requirements of Fishes Brett, J. R. The Quarterly Review of Biology, Vol. 31, Issue 2 https://doi.org/10.1086/401257	journal	June 1956
Heat Shock Changes the Heterogeneity Distribution in Populations of Caenorhabditis elegans: Does It Tell Us Anything About the Biological Mechanism of Stress Response? Yashin, A. I.; Cypser, J. W.; Johnson, T. E. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, Vol. 57, Issue 3 https://doi.org/10.1093/gerona/57.3.B83	journal	March 2002
Heat Shock Responses of Closely Related Species of Tropical and Desert Fish Hightower, Lawrence E.; Norris, Carol E.; Diiorio, Philip J. American Zoologist, Vol. 39, Issue 6 https://doi.org/10.1093/icb/39.6.877	journal	December 1999
Stress in Fishes: A Diversity of Responses with Particular Reference to Changes in Circulating Corticosteroids Barton, B. A. Integrative and Comparative Biology, Vol. 42, Issue 3 https://doi.org/10.1093/icb/42.3.517	journal	July 2002
Survival bottlenecks in the early ontogenesis of Atlantic herring (Clupea harengus, L.) in coastal lagoon spawning areas of the western Baltic Sea Polte, Patrick; Kotterba, Paul; Hammer, Cornelius ICES Journal of Marine Science, Vol. 71, Issue 4 https://doi.org/10.1093/icesjms/fst050	journal	May 2013
Defining individual quality over lifetimes and selective contexts Lailvaux, Simon P.; Kasumovic, Michael M. Proceedings of the Royal Society B: Biological Sciences, Vol. 278, Issue 1704 https://doi.org/10.1098/rspb.2010.1591	journal	September 2010
Travelling on a budget: predictions and ecological evidence for bottlenecks in the annual cycle of long-distance migrants Buehler, Deborah M.; Piersma, Theunis Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1490 https://doi.org/10.1098/rstb.2007.2138	journal	July 2007
Age, stage and senescence in plants Caswell, Hal; Salguero‐Gómez, Roberto Journal of Ecology, Vol. 101, Issue 3 https://doi.org/10.1111/1365-2745.12088	journal	April 2013
The Contribution of Phenotypic Plasticity to Adaptation in Lacerta Vivipara Lorenzon, Pauline; Clobert, Jean; Massot, Manuel Evolution, Vol. 55, Issue 2 https://doi.org/10.1111/j.0014-3820.2001.tb01302.x	journal	February 2001
Energetics and morphology of sockeye salmon: effects of upriver migratory distance and elevation Crossin, G. T.; Hinch, S. G.; Farrell, A. P. Journal of Fish Biology, Vol. 65, Issue 3 https://doi.org/10.1111/j.0022-1112.2004.00486.x	journal	September 2004
Endurance of simulated winter conditions by age-0 walleye pollock: effects of body size, water temperature and energy stores Sogard, S. M.; Olla, B. L. Journal of Fish Biology, Vol. 56, Issue 1 https://doi.org/10.1111/j.1095-8649.2000.tb02083.x	journal	January 2000
Causes and consequences of winter mortality in fishes Hurst, T. P. Journal of Fish Biology, Vol. 71, Issue 2 https://doi.org/10.1111/j.1095-8649.2007.01596.x	journal	August 2007
Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities Duarte, Helder; Tejedo, Miguel; Katzenberger, Marco Global Change Biology, Vol. 18, Issue 2 https://doi.org/10.1111/j.1365-2486.2011.02518.x	journal	September 2011
Independence among physiological traits suggests flexibility in the face of ecological demands on phenotypes Buehler, D. M.; VÉZina, F.; Goymann, W. Journal of Evolutionary Biology, Vol. 25, Issue 8 https://doi.org/10.1111/j.1420-9101.2012.02543.x	journal	June 2012
Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Bowler, Ken; Terblanche, John S. Biological Reviews, Vol. 83, Issue 3 https://doi.org/10.1111/j.1469-185X.2008.00046.x	journal	August 2008
Interacting Effects of Phenotypic Plasticity and Evolution on Population Persistence in a Changing Climate: Evolution, Plasticity, and Climate Change Reed, Thomas E.; Schindler, Daniel E.; Waples, Robin S. Conservation Biology, Vol. 25, Issue 1 https://doi.org/10.1111/j.1523-1739.2010.01552.x	journal	July 2010
Climate Warming and Disease Risks for Terrestrial and Marine Biota Harvell, C. D. Science, Vol. 296, Issue 5576 https://doi.org/10.1126/science.1063699	journal	June 2002
An experimental examination of temperature interactions in the match–mismatch hypothesis for Pacific cod larvae Laurel, Benjamin J.; Hurst, Thomas P.; Ciannelli, Lorenzo Canadian Journal of Fisheries and Aquatic Sciences, Vol. 68, Issue 1 https://doi.org/10.1139/F10-130	journal	January 2011
Levels of stored energy but not marine foraging patterns differentiate seasonal ecotypes of wild and hatchery steelhead (Oncorhynchus mykiss) returning to the Kalama River, Washington Lamperth, James S.; Quinn, Thomas P.; Zimmerman, Mara S. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 74, Issue 2 https://doi.org/10.1139/cjfas-2016-0018	journal	February 2017
Atlantic salmon (Salmo salar) in winter: "the season of parr discontent"? Cunjak, R. A.; Prowse, T. D.; Parrish, D. L. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 55, Issue S1 https://doi.org/10.1139/d98-008	journal	January 1998
The effects of environmental heat stress on heat-shock mRNA and protein expression in Miramichi Atlantic salmon (Salmo salar) parr Lund, Susan G.; Caissie, Daniel; Cunjak, Richard A. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 59, Issue 9 https://doi.org/10.1139/f02-117	journal	September 2002
Over-winter lipid depletion and mortality of age-0 rainbow trout (Oncorhynchusmykiss) Biro, Peter A.; Morton, Ashley E.; Post, John R. Canadian Journal of Fisheries and Aquatic Sciences, Vol. 61, Issue 8 https://doi.org/10.1139/f04-083	journal	August 2004
Temperature Tolerance in Young Pacific Salmon, Genus Oncorhynchus Brett, J. R. Journal of the Fisheries Research Board of Canada, Vol. 9, Issue 6 https://doi.org/10.1139/f52-016	journal	June 1952
Effect of Thermal Shock on Vulnerability of Juvenile Salmonids to Predation Coutant, Charles C. Journal of the Fisheries Research Board of Canada, Vol. 30, Issue 7 https://doi.org/10.1139/f73-157	journal	July 1973
Effects of Constant Temperatures and Diel Temperature Fluctuations on Specific Growth and Mortality Rates and Yield of Juvenile Rainbow Trout, Salmo gairdneri Hokanson, Kenneth E. F.; Kleiner, Charles F.; Thorslund, Todd W. Journal of the Fisheries Research Board of Canada, Vol. 34, Issue 5 https://doi.org/10.1139/f77-100	journal	May 1977
Temperature Requirements of Some Percids and Adaptations to the Seasonal Temperature Cycle Hokanson, Kenneth E. F. Journal of the Fisheries Research Board of Canada, Vol. 34, Issue 10 https://doi.org/10.1139/f77-217	journal	October 1977
The dead of winter: size-dependent variation and genetic differences in seasonal mortality among Atlantic silverside (Atherinidae: Menidia menidia) from different latitudes Schultz, Eric T.; Conover, David O.; Ehtisham, Amir Canadian Journal of Fisheries and Aquatic Sciences, Vol. 55, Issue 5 https://doi.org/10.1139/f97-320	journal	May 1998
Secondary sexual characters, energy use, senescence, and the cost of reproduction in sockeye salmon Hendry, Andrew P.; Berg, Ole K. Canadian Journal of Zoology, Vol. 77, Issue 11 https://doi.org/10.1139/z99-158	journal	December 1999
Temperature Compensation Fry, F. E. J. Annual Review of Physiology, Vol. 20, Issue 1 https://doi.org/10.1146/annurev.ph.20.030158.001231	journal	March 1958
OXIDATIVE STRESS IN MARINE ENVIRONMENTS: Biochemistry and Physiological Ecology Lesser, Michael P. Annual Review of Physiology, Vol. 68, Issue 1 https://doi.org/10.1146/annurev.physiol.68.040104.110001	journal	January 2006
Heat Waves, the New Normal: Summertime Temperature Extremes Will Impact Animals, Ecosystems, and Human Communities Stillman, Jonathon H. Physiology, Vol. 34, Issue 2 https://doi.org/10.1152/physiol.00040.2018	journal	March 2019
Intraspecific variation in thermal tolerance and heat shock protein gene expression in common killifish, Fundulus heteroclitus Fangue, N. A. Journal of Experimental Biology, Vol. 209, Issue 15 https://doi.org/10.1242/jeb.02260	journal	August 2006
Responses to temperature variation: integration of thermoregulation and metabolism in vertebrates Seebacher, Frank Journal of Experimental Biology, Vol. 212, Issue 18 https://doi.org/10.1242/jeb.024430	journal	September 2009
Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology Pörtner, Hans-O.; Bock, Christian; Mark, Felix C. The Journal of Experimental Biology, Vol. 220, Issue 15 https://doi.org/10.1242/jeb.134585	journal	August 2017
Physiological disturbances at critically high temperatures: a comparison between stenothermal antarctic and eurythermal temperate eelpouts (Zoarcidae) van Dijk, P. L.; Tesch, C.; Hardewig, I. Journal of Experimental Biology, Vol. 202, Issue 24 https://doi.org/10.1242/jeb.202.24.3611	journal	December 1999
Thermal Resistance of Rainbow Trout from a Permanently Heated Stream, and of Two Hatchery Strains Kaya, Calvin M. The Progressive Fish-Culturist, Vol. 40, Issue 4 https://doi.org/10.1577/1548-8659(1978)40[138:TRORTF]2.0.CO;2	journal	October 1978
Size-Dependent Effects of Continuous and Intermittent Feeding on Starvation Time and Mass Loss in Starving Yellow Perch Larvae and Juveniles Letcher, Benjamin H.; Rice, James A.; Crowder, Larry B. Transactions of the American Fisheries Society, Vol. 125, Issue 1 https://doi.org/10.1577/1548-8659(1996)125<0014:SDEOCA>2.3.CO;2	journal	January 1996
Relative Importance of Direct and Indirect Effects of Starvation for Young Walleyes Jonas, Jory L.; Wahl, David H. Transactions of the American Fisheries Society, Vol. 127, Issue 2 https://doi.org/10.1577/1548-8659(1998)127<0192:RIODAI>2.0.CO;2	journal	March 1998
Influence of Predation Risk on the Overwinter Mortality and Energetic Relationships of Young-of-Year Walleyes Pratt, Thomas C.; Fox, Michael G. Transactions of the American Fisheries Society, Vol. 131, Issue 5 https://doi.org/10.1577/1548-8659(2002)131<0885:IOPROT>2.0.CO;2	journal	September 2002
Disease Susceptibility of Hatchery Snake River Spring–Summer Chinook Salmon with Different Juvenile Migration Histories in the Columbia River Arkoosh, Mary R.; Kagley, Anna N.; Anulacion, Bernadita F. Journal of Aquatic Animal Health, Vol. 18, Issue 4 https://doi.org/10.1577/H05-051.1	journal	December 2006
Effects of River Discharge, Temperature, and Future Climates on Energetics and Mortality of Adult Migrating Fraser River Sockeye Salmon Rand, P. S.; Hinch, S. G.; Morrison, J. Transactions of the American Fisheries Society, Vol. 135, Issue 3 https://doi.org/10.1577/T05-023.1	journal	May 2006
Comparative Thermal Requirements of Westslope Cutthroat Trout and Rainbow Trout: Implications for Species Interactions and Development of Thermal Protection Standards Bear, Elizabeth A.; McMahon, Thomas E.; Zale, Alexander V. Transactions of the American Fisheries Society, Vol. 136, Issue 4 https://doi.org/10.1577/T06-072.1	journal	July 2007
A Vitality-Based Model Relating Stressors and Environmental Properties to Organism Survival Anderson, James J. Ecological Monographs, Vol. 70, Issue 3 https://doi.org/10.1890/0012-9615(2000)070[0445:AVBMRS]2.0.CO;2	journal	June 2000
Energy Allocation Strategy in Young Fish: Allometry and Survival Post, John R.; Parkinson, E. A. Ecology, Vol. 82, Issue 4 https://doi.org/10.1890/0012-9658(2001)082[1040:EASIYF]2.0.CO;2	journal	April 2001
From Stage to age in Variable Environments: life Expectancy and Survivorship Tuljapurkar, Shripad; Horvitz, Carol C. Ecology, Vol. 87, Issue 6 https://doi.org/10.1890/0012-9658(2006)87[1497:FSTAIV]2.0.CO;2	journal	June 2006
Juvenile mortality in benthic marine invertebrates Gosselin, La; Qian, Py Marine Ecology Progress Series, Vol. 146 https://doi.org/10.3354/meps146265	journal	January 1997

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Title: Step-patterned survivorship curves: Mortality and loss of equilibrium responses to high temperature and food restriction in juvenile rainbow trout (Oncorhynchus mykiss)

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