Climate variability and life history impact stress, thyroid, and immune markers in California sea lions (Zalophus californianus) during El Nino conditions.

De Rango E, Prager KC, Greig DJ, Hooper AW, Crocker DE (2019)
Conservation physiology 7(1): coz010.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
De Rango, EugeneUniBi; Prager, Katherine C; Greig, Denise J; Hooper, Amanda W; Crocker, Daniel E
Abstract / Bemerkung
Wildlife is exposed to a diverse set of extrinsic and intrinsic stressors, such as climatic variation or life history constraints, which may impact individual health and fitness. El Nino and climatic anomalies between 2013 and 2016 had major ecological impacts on the California Current ecosystem. As top marine predators, California sea lions (CSL) experienced decreased prey availability and foraging success, impacting their nutritional state. We hypothesize that chronic stress to juvenile CSL increased during the 2015-2016 El Nino and that breeding represents a period of chronic stress for adults, which impact a variety of physiological processes. We opportunistically captured and sampled juvenile CSL (female, n=29; male, n=38) in central California and adult male CSL (n=76) in Astoria, Oregon and quantified a suite of analytes in serum as indicators of acute stress markers, metabolism and thyroid function, and adaptive immune response. We found that stress hormones and glucose were decreased in juvenile CSL during 2016 relative to 2015 and in adult male CSL after the breeding season, which may indicate chronic stress downregulating HPA (hypothalamic-pituitary-adrenal) axis sensitivity with associated metabolic impacts. Conversely, thyroid hormones for both juvenile and adult male CSL were increased, suggesting greater energetic requirements resulting from increased foraging activity during suboptimal conditions in juveniles and breeding tenure in adult males. Immunoglobulin IgG was elevated in juveniles in 2016 but reduced in adult males post-breeding. This suggests that juveniles may face immunostimulatory pressure during anomalously warm ocean environments; however, for adult males, breeding is a significant energetic cost resulting in reductions to immune function. Our results indicate that environmental conditions and life history stage may influence physiological responses in an important marine predator and a sentinel species of changing ocean ecosystems.
Conservation physiology
Page URI


De Rango E, Prager KC, Greig DJ, Hooper AW, Crocker DE. Climate variability and life history impact stress, thyroid, and immune markers in California sea lions (Zalophus californianus) during El Nino conditions. Conservation physiology. 2019;7(1): coz010.
De Rango, E., Prager, K. C., Greig, D. J., Hooper, A. W., & Crocker, D. E. (2019). Climate variability and life history impact stress, thyroid, and immune markers in California sea lions (Zalophus californianus) during El Nino conditions. Conservation physiology, 7(1), coz010. doi:10.1093/conphys/coz010
De Rango, E., Prager, K. C., Greig, D. J., Hooper, A. W., and Crocker, D. E. (2019). Climate variability and life history impact stress, thyroid, and immune markers in California sea lions (Zalophus californianus) during El Nino conditions. Conservation physiology 7:coz010.
De Rango, E., et al., 2019. Climate variability and life history impact stress, thyroid, and immune markers in California sea lions (Zalophus californianus) during El Nino conditions. Conservation physiology, 7(1): coz010.
E. De Rango, et al., “Climate variability and life history impact stress, thyroid, and immune markers in California sea lions (Zalophus californianus) during El Nino conditions.”, Conservation physiology, vol. 7, 2019, : coz010.
De Rango, E., Prager, K.C., Greig, D.J., Hooper, A.W., Crocker, D.E.: Climate variability and life history impact stress, thyroid, and immune markers in California sea lions (Zalophus californianus) during El Nino conditions. Conservation physiology. 7, : coz010 (2019).
De Rango, Eugene, Prager, Katherine C, Greig, Denise J, Hooper, Amanda W, and Crocker, Daniel E. “Climate variability and life history impact stress, thyroid, and immune markers in California sea lions (Zalophus californianus) during El Nino conditions.”. Conservation physiology 7.1 (2019): coz010.

99 References

Daten bereitgestellt von Europe PubMed Central.

Effects of environmental change on wildlife health.
Acevedo-Whitehouse K, Duffus AL., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 364(1534), 2009
PMID: 19833653
Stress physiology in marine mammals: how well do they fit the terrestrial model?
Atkinson S, Crocker D, Houser D, Mashburn K., J. Comp. Physiol. B, Biochem. Syst. Environ. Physiol. 185(5), 2015
PMID: 25913694
Climatic anomaly affects the immune competence of California sea lions
Banuet-Martínez M, Espinosa-de W, Elorriaga-Verplancken FR, Flores-Morán A, García OP, Camacho M, Acevedo-Whitehouse K., 2017
Evidence of anthropogenic trauma in marine mammals stranded along the central California coast, 2003–2015
Barcenas-De D, DeRango E, Johnson SP, Simeone CA., 2018
Reality as the leading cause of stress: rethinking the impact of chronic stress in nature
Boonstra R., 2013
Applying the tools of ecological immunology to conservation: a test case in the Galápagos sea lion
Brock P, Hall A, Goodman S, Cruz M, Acevedo-Whitehouse K., 2013
Immune activity, body condition and human-associated environmental impacts in a wild marine mammal
Brock PM, Hall AJ, Goodman SJ, Cruz M, Acevedo-Whitehouse K., 2013
Increasing frequency of extreme El Niño events due to greenhouse warming
Cai W, Borlace S, Lengaigne M, Van P, Collins M, Vecchi G, Timmermann A, Santoso A, McPhaden MJ, Wu L., 2014
The effects of handling and anesthetic agents on the stress response and carbohydrate metabolism in northern elephant seals
Champagne CD, Houser DS, Costa DP, Crocker DE., 2012
A profile of carbohydrate metabolites in the fasting northern elephant seal.
Champagne CD, Boaz SM, Fowler MA, Houser DS, Costa DP, Crocker DE., Comp. Biochem. Physiol. Part D Genomics Proteomics 8(2), 2013
PMID: 23542762
Adrenal sensitivity to stress is maintained despite variation in baseline glucocorticoids in moulting seals.
Champagne C, Tift M, Houser D, Crocker D., Conserv Physiol 3(1), 2015
PMID: 27293689
Comprehensive endocrine response to acute stress in the bottlenose dolphin from serum, blubber, and feces.
Champagne CD, Kellar NM, Trego ML, Delehanty B, Boonstra R, Wasser SK, Booth RK, Crocker DE, Houser DS., Gen. Comp. Endocrinol. 266(), 2018
PMID: 29852162
Endocrinology of the stress response.
Charmandari E, Tsigos C, Chrousos G., Annu. Rev. Physiol. 67(), 2005
PMID: 15709959
Lactation and resource limitation affect stress responses, thyroid hormones, immune function, and antioxidant capacity of sea otters (Enhydra lutris)
Chinn SM, Monson DH, Tinker MT, Staedler MM, Crocker DE., 2018
Stress and disorders of the stress system.
Chrousos GP., Nat Rev Endocrinol 5(7), 2009
PMID: 19488073
Global patterns and impacts of El Niño events on coral reefs: a meta-analysis
Claar DC, Szostek L, McDevitt-Irwin JM, Schanze JJ, Baum JK., 2018
Variation within and between birds in corticosterone responses of great tits (Parus major).
Cockrem JF, Silverin B., Gen. Comp. Endocrinol. 125(2), 2002
PMID: 11884065

Cooper D, Ladenson P., 2011
Reproductive and foraging energetics of high latitude penguins, albatrosses and pinnipeds: implications for life history patterns
Costa DP., 1991

Costa D, Antonelis G, DeLong R., 1991
Impact of El Niño on the foraging behavior of female northern elephant seals
Crocker DE, Costa DP, Le BJ, Webb PM, Houser DS., 2006
Hormone and metabolite changes associated with extended breeding fasts in male northern elephant seals (Mirounga angustirostris).
Crocker DE, Ortiz RM, Houser DS, Webb PM, Costa DP., Comp. Biochem. Physiol., Part A Mol. Integr. Physiol. 161(4), 2011
PMID: 22227222
The role of thyroid hormones in the control of energy expenditure.
Danforth E Jr, Burger A., Clin Endocrinol Metab 13(3), 1984
PMID: 6391756
Age-and sex-specific survival of California Sea lions (Zalophus californianus) at San Miguel island, California
DeLong RL, Melin SR, Laake JL, Morris P, Orr AJ, Harris JD., 2017
Response to capture stress involves multiple corticosteroids and is associated with serum thyroid hormone concentrations in Guadalupe fur seals (Arctocephalus philippii townsendi)
DeRango EJ, Greig DJ, Gálvez C, Norris TA, Barbosa L, Elorriaga-Verplancken FR, Crocker DE., 2018
Impact of the 2015 El Niño-southern oscillation on the abundance and foraging habits of Guadalupe fur seals and California sea lions from the San Benito archipelago, Mexico
Elorriaga-Verplancken FR, Sierra-Rodríguez GE, Rosales-Nanduca H, Acevedo-Whitehouse K, Sandoval-Sierra J., 2016
Evolution and historical perspective of the 1997–1998 El Niño–southern oscillation event
Enfield DB., 2001
Metabolic responses to adrenocorticotropic hormone (ACTH) vary with life-history stage in adult male northern elephant seals.
Ensminger DC, Somo DA, Houser DS, Crocker DE., Gen. Comp. Endocrinol. 204(), 2014
PMID: 24798580
Serum free and total iodothyronine concentrations in dogs with hyperadrenocorticism.
Ferguson DC, Peterson ME., Am. J. Vet. Res. 53(9), 1992
PMID: 1416369
Atypical Red Blood Cells Are Prevalent in California Sea Lion Pups Born during Anomalous Sea Surface Temperature Events.
Flores-Moran A, Banuet-Martinez M, Elorriaga-Verplancken FR, Garcia-Ortuno LE, Sandoval-Sierra J, Acevedo-Whitehouse K., Physiol. Biochem. Zool. 90(5), 2017
PMID: 28671858
A decade of live California sea lion (Zalophus californianus) strandings along the central California coast: causes and trends, 1991-2000
Greig DJ, Gulland FM, Kreuder C., 2005
Evaluation of circulating eosinophil count and adrenal gland function in California sea lions naturally exposed to domoic acid.
Gulland FM, Hall AJ, Greig DJ, Frame ER, Colegrove KM, Booth RK, Wasser SK, Scott-Moncrieff JC., J. Am. Vet. Med. Assoc. 241(7), 2012
PMID: 23013509
New paradigms for supporting the resilience of marine ecosystems.
Hughes TP, Bellwood DR, Folke C, Steneck RS, Wilson J., Trends Ecol. Evol. (Amst.) 20(7), 2005
PMID: 16701400
Impacts of the 2015–2016 El Niño on the California current system: early assessment and comparison to past events
Jacox MG, Hazen EL, Zaba KD, Rudnick DL, Edwards CA, Moore AM, Bograd SJ., 2016
Global threats to pinnipeds
Kovacs KM, Aguilar A, Aurioles D, Burkanov V, Campagna C, Gales N, Gelatt T, Goldsworthy SD, Goodman SJ, Hofmeyr GJ., 2012
Interannual variation in the at-sea behavior of California sea lions (Zalophus californianus)
Kuhn CE, Costa DP., 2014
California sea lion sex- and age-specific morphometry
Laake JL, Melin SR, Orr AJ, Greig DG, Prager KC, DeLong RL, Harris JD., 2016
Population growth and status of California sea lions
Laake JL, Lowry MS, DeLong RL, Melin SR, Carretta JV., 2018
State of the California current 2013–14: El Niño looming
Leising AW, Schroeder ID, Bograd SJ, Bjorkstedt EP, Field J, Sakuma K, Abell J, Robertson RR, Tyburczy J, Peterson WT., 2014

Leising AW, Schroeder ID, Bograd SJ, Abell J, Durazo R, Gaxiola-Castro G, Bjorkstedt EP, Field J, Sakuma K, Robertson RR., 2015
Recent collapse of northern anchovy biomass off California
MacCall AD, Sydeman WJ, Davison PC, Thayer JA., 2016
Immunological memory is compromised by food restriction in deer mice Peromyscus maniculatus.
Martin LB 2nd, Navara KJ, Weil ZM, Nelson RJ., Am. J. Physiol. Regul. Integr. Comp. Physiol. 292(1), 2006
PMID: 16902185
Cumulative human impacts on marine predators
Maxwell SM, Hazen EL, Bograd SJ, Halpern BS, Breed GA, Nickel B, Teutschel NM, Crowder LB, Benson S, Dutton PH., 2013
Food limitation of sea lion pups and the decline of forage off central and southern California.
McClatchie S, Field J, Thompson AR, Gerrodette T, Lowry M, Fiedler PC, Watson W, Nieto KM, Vetter RD., R Soc Open Sci 3(3), 2016
PMID: 27069651
Conservation endocrinology
McCormick SD, Romero LM., 2017
Repeated adrenocorticotropic hormone administration alters adrenal and thyroid hormones in free-ranging elephant seals.
McCormley MC, Champagne CD, Deyarmin JS, Stephan AP, Crocker DE, Houser DS, Khudyakov JI., Conserv Physiol 6(1), 2018
PMID: 30034809
Trade-offs between acquired and innate immune defenses in humans.
McDade TW, Georgiev AV, Kuzawa CW., Evol Med Public Health 2016(1), 2016
PMID: 26739325
Stress and the individual. Mechanisms leading to disease.
McEwen BS, Stellar E., Arch. Intern. Med. 153(18), 1993
PMID: 8379800
The role of adrenocorticoids as modulators of immune function in health and disease: neural, endocrine and immune interactions.
McEwen BS, Biron CA, Brunson KW, Bulloch K, Chambers WH, Dhabhar FS, Goldfarb RH, Kitson RP, Miller AH, Spencer RL, Weiss JM., Brain Res. Brain Res. Rev. 23(1-2), 1997
PMID: 9063588
Energy and prey requirements of California sea lions under variable environmental conditions
McHuron E, Mangel M, Schwarz L, Costa D., 2017
Movements and dive behavior of juvenile California sea lions from Año Nuevo Island
McHuron EA, Block BA, Costa DP., 2018
A state-dependent model for assessing the population consequences of disturbance on income-breeding mammals
McHuron EA, Schwarz LK, Costa DP, Mangel M., 2018
Effects of glucocorticoids on carbohydrate metabolism.
McMahon M, Gerich J, Rizza R., Diabetes Metab Rev 4(1), 1988
PMID: 3278872
The effects of El Niño on the foraging behavior of lactating California sea lions (Zalophus californianus californianus) during the nonbreeding season
Melin S, DeLong R, Siniff D., 2008
Unprecedented mortality of California sea lion pups associated with anomalous oceanographic conditions along the central California coast in 2009
Melin SR, Orr AJ, Harris JD, Laake JL, Delong RL, Gulland F, Stoudt S., 2009
Reversible immobilization of free-ranging adult male California sea lions (Zalophus californianus)
Melin SR, Haulena M, Bonn W, Tennis MJ, Brown RF, Harris JD., 2013
State of the Climate: National Climate Report for Annual
Approaches to understanding the cumulative effects of stressors on marine mammals
The effect of a natural environmental disturbance on maternal investment and pup behavior in the California sea lion
Ono KA, Boness DJ, Oftedal OT., 1987
Glucose metabolism regulates T cell activation, differentiation, and functions.
Palmer CS, Ostrowski M, Balderson B, Christian N, Crowe SM., Front Immunol 6(), 2015
PMID: 25657648
Body reserves influence allocation to immune responses in capital breeding female northern elephant seals
Peck HE, Costa DP, Crocker DE., 2016
Serum cortisol in California sea lion pups (Zalophus californianus californianus)
Pedernera-Romano C, Aurioles-Gamboa D, Valdez R, Brousset D, Romano M, Galindo F., 2010

Peterson W, Robert M, Bond N., 2015
On the adaptive significance of stress-induced immunosuppression
Råberg L, Grahn M, Hasselquist D, Svensson E., 1998
Exposure to chronic stress downregulates corticosterone responses to acute stressors
Rich EL, Romero LM., 2005

Riedman M., 1990
Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events.
Romero LM, Wikelski M., Proc. Natl. Acad. Sci. U.S.A. 98(13), 2001
PMID: 11416210
The Reactive Scope Model - a new model integrating homeostasis, allostasis, and stress.
Romero LM, Dickens MJ, Cyr NE., Horm Behav 55(3), 2009
PMID: 19470371

Romero LM, Wingfield JC., 2015
Immune function in free-ranging harbor seal (Phoca vitulina) mothers and their pups during lactation.
Ross PS, Pohajdak B, Bowen WD, Addison RF., J. Wildl. Dis. 29(1), 1993
PMID: 8445787
Immune-mediated hookworm clearance and survival of a marine mammal decrease with warmer ocean temperatures.
Seguel M, Montalva F, Perez-Venegas D, Gutierrez J, Paves HJ, Muller A, Valencia-Soto C, Howerth E, Mendiola V, Gottdenker N., Elife 7(), 2018
PMID: 30398149
Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology.
Sheldon BC, Verhulst S., Trends Ecol. Evol. (Amst.) 11(8), 1996
PMID: 21237861
A systematic review of changes in marine mammal health in North America, 1972-2012: the need for a novel integrated approach
Simeone CA, Gulland FM, Norris T, Rowles TK., 2015
Changes in diet and maternal attendance of south American sea lions indicate changes in the marine environment and prey abundance
Soto KH, Trites AW, Arias-Schreiber M., 2006
The definition of El Niño
Trenberth KE., 1997
The behavioral ecology of maternal effort in fur seals and sea lions
Trillmich F., 1990
Drastic effects of El Nino on Galapagos pinnipeds.
Trillmich F, Limberger D., Oecologia 67(1), 1985
PMID: 28309839

Trillmich F, Ono K, Costa D, DeLong R, Feldkamp S, Francis J, Gentry RL, Heath C, LeBoeuf B, Majluf P., 1991
Marine algal toxins: origins, health effects, and their increased occurrence.
Van Dolah FM., Environ. Health Perspect. 108 Suppl 1(), 2000
PMID: 10698729
Movement and diving behavior of male California Sea lion (Zalophus californianus) during anomalous oceanographic conditions of 2005 compared to those of 2004
Weise MJ, Costa DP, Kudela RM., 2006
Temporal variability in ocean climate and California sea lion diet and biomass consumption: implications for fisheries management
Weise MJ, Harvey JT., 2008
Conservation physiology.
Wikelski M, Cooke SJ., Trends Ecol. Evol. (Amst.) 21(1), 2005
PMID: 16701468
The comparative biology of environmental stress: behavioural endocrinology and variation in ability to cope with novel, changing environments
Wingfield JC., 2013

Wingfield JC, Hunt K, Breuner C, Dunlap K, Fowler GS, Freed L, Lepson J., 1997
Hormone-behavior interrelationships of birds in response to weather
Wingfield JC, Ramenofsky M., 2011
Effects of El Nino and La Nina Southern Oscillation events on the adrenocortical responses to stress in birds of the Galapagos Islands.
Wingfield JC, Hau M, Boersma PD, Romero LM, Hillgarth N, Ramenofsky M, Wrege P, Scheibling R, Kelley JP, Walker B, Wikelski M., Gen. Comp. Endocrinol. 259(), 2017
PMID: 29106968
Movements of male California sea lions captured in the Columbia River
Wright BE, Tennis MJ, Brown RF., 2010
The physiology of life history trade-offs in animals
Zera AJ, Harshman LG., 2001


Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®


PMID: 31110762
PubMed | Europe PMC

Suchen in

Google Scholar