Skip to main content

Physiological Thresholds in the Context of Marine Mammal Conservation

  • Chapter
  • First Online:
Reproductive Sciences in Animal Conservation

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1200))

  • 2117 Accesses

Abstract

There is growing evidence of the adverse effects of global environmental change on marine mammals, particularly in terms of changes in abundance, distribution, habitat use, migratory phenology, feeding habits, risk of infectious diseases, bioaccumulation of contaminants, declines in reproductive success, and reductions in genetic diversity. These anthropogenic stressors have led to an evident conservation crisis: a quarter of the extant marine mammal species that have been assessed and now considered at risk of extinction. However, we still know very little about the subtle, subclinical effects of environmental stressors on various aspects of physiology that could impacts their survival and long-term fertility, or that could impact the performance of future generations. This chapter argues for the need of considering physiological thresholds when examining how drivers of global environmental change can impact marine mammal populations. It also poses questions regarding our understanding of individual phenotypic plasticity and resilience of species in the face of environmental stressors, particularly under abrupt and unpredictable environmental changes. Specifically, I present evidence of how drivers of environmental change can exert effects at different levels of biological organization to influence the viability of individuals and populations, and discuss which aspects of environmental change could be the most likely to shift the physiological thresholds of different marine mammal species. Finally, the chapter identifies areas of further research in marine mammal conservation physiology in the current context of global environmental change.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Acevedo-Whitehouse K, Bowen L. Genetics. In: Dierauf L, Gulland FMD, editors. RC handbook of marine mammal medicine: health, disease and rehabilitation. 3rd ed. Boca Raton: CRC Press; 2018. p. 231–48.

    Google Scholar 

  • Acevedo-Whitehouse K, Cunningham AA. Is MHC enough for understanding wildlife immunogenetics? Trends Ecol Evol. 2006;21:433–8.

    Article  PubMed  Google Scholar 

  • Acevedo-Whitehouse K, Duffus ALJ. Effects of environmental change on wildlife health. Philos Trans R Soc Lond B Biol Sci. 2009;364(1534):3429–38.

    Article  PubMed  PubMed Central  Google Scholar 

  • Acevedo-Whitehouse K, Gulland F, Greig D, Amos W. Inbreeding: disease susceptibility in California sea lions. Nature. 2003;422(6927):35.

    Article  CAS  PubMed  Google Scholar 

  • Acevedo-Whitehouse K, Spraker TR, Lyons E, Melin SR, Gulland F, Delong RL, et al. Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups. Mol Ecol. 2006;15(7):1973–82.

    Article  CAS  PubMed  Google Scholar 

  • Acevedo-Whitehouse K, Rocha-Gosselin A, Gendron D. A novel non-invasive tool for disease surveillance of free-ranging whales and its relevance to conservation programs. Anim Conserv. 2010;13(2):217–25.

    Article  Google Scholar 

  • Alava JJ, Palomera C, Bendell L, Ross PS. Pollution as a threat for the conservation of the Galapagos marine reserve: environmental impacts and management perspectives. In: Denkinger J, Vinueza L, editors. The Galapagos marine reserve: a dynamic socio-ecological system. New York: Springer; 2014. p. 247–83.

    Chapter  Google Scholar 

  • Altimiras J, Anderson WG. Ecophysiology methods: refining the old, validating the new and developing for the future. Comp Biochem Physiol A Mol Integr Physiol. 2016;202:1–2.

    Article  CAS  PubMed  Google Scholar 

  • Apprill A, Miller CA, Moore MJ, Durban JW, Fearnbach H, Barrett-Lennard LG. Extensive core microbiome in drone-captured whale blow supports a framework for health monitoring. mSystems. 2017;2(5):e00119–7.

    Article  PubMed  PubMed Central  Google Scholar 

  • Banuet-Martínez M, Espinosa-de-Aquino W, Elorriaga-Verplancken FR, Flores-Morán A, García OP, Camacho M, et al. Climatic anomaly affects the immune competence of California sea lions. PLoS One. 2017;12(6):0179359.

    Article  CAS  Google Scholar 

  • Baris HN, Barnes-Kedar I, Toledano H, Halpern M, Hershkovitz D, Lossos A, et al. Constitutional mismatch repair deficiency in Israel: high proportion of founder mutations in MMR genes and consanguinity. Pediatr Blood Cancer. 2016;6(3):418–27.

    Article  CAS  Google Scholar 

  • Barnosky AD, Matzke N, Tomiya S, Wogan GO, Swartz B, Quental TB, et al. Has the earth’s sixth mass extinction already arrived? Nature. 2011;471(7336):51–7.

    Article  CAS  PubMed  Google Scholar 

  • Bean K, Amos W, Pomeroy PP, Twiss SD, Coulson TN, Boyd IL. Patterns of parental relatedness and pup survival in the grey seal (Halichoerus grypus). Mol Ecol. 2004;13(8):2365–70.

    Article  CAS  PubMed  Google Scholar 

  • Bellard C, Cassey P, Blackburn TM. Alien species as a driver of recent extinctions. Biol Lett. 2016;12:20150623.

    Article  PubMed  PubMed Central  Google Scholar 

  • Berta A, Sumich JL, Kovacs KM. Marine mammals: evolutionary biology. 3rd ed. Amsterdam: Academic Press; 2015.

    Google Scholar 

  • Bijlsma R, Loeschcke V. Genetic erosion impedes adaptive responses to stressful environments. Evol Appl. 2012;5(2):117–29.

    Article  CAS  PubMed  Google Scholar 

  • Block BA, Jonsen ID, Jorgensen SJ, Winship AJ, Shaffer SA, Bograd SJ, et al. Tracking apex marine predator movements in a dynamic ocean. Nature. 2011;475(7354):86–90.

    Article  CAS  PubMed  Google Scholar 

  • Botero CA, Weissing FJ, Wright J, Rubenstein DR. Evolutionary tipping points in the capacity to adapt to environmental change. Proc Natl Acad Sci. 2014;112(1):184–9.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bowen L, Miles AK, Murray M, Haulena M, Tuttle J, van Bonn W, et al. Gene transcription in sea otters (Enhydra lutris); development of a diagnostic tool for sea otter and ecosystem health. Mol Ecol Resour. 2012;12:67–74.

    Article  CAS  PubMed  Google Scholar 

  • Brock PM, Goodman SJ, Hall AJ, Cruz M, Acevedo-Whitehouse K. Context-dependent associations between heterozygosity and immune variation in a wild carnivore. BMC Evol Biol. 2015;15(242):1–10.

    Google Scholar 

  • Brown TM, Hammond SA, Behsaz B, Veldhoen N, Birol I, Helbing CC. De novo assembly of the ringed seal (Pusa hispida) blubber transcriptome: a tool that enables identification of molecular health indicators associated with PCB exposure. Aquat Toxicol. 2017;185:48–57.

    Article  CAS  PubMed  Google Scholar 

  • Burek KA, Gulland FMD, O’Hara TM. Effects of climate change on arctic ecosystems. Ecol Appl. 2008;18(2):S126–34.

    Article  PubMed  Google Scholar 

  • Burgess EA, Hunt KE, Kraus SD, Rolland RM. Quantifying hormones in exhaled breath for physiological assessment of large whales at sea. Sci Rep. 2018;8(1):10031.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Casas-Marce M, Soriano L, López-Bao JV, Godoy JA. Genetics at the verge of extinction: insights from the Iberian lynx. Mol Ecol. 2013;22(22):5503–15.

    Article  CAS  PubMed  Google Scholar 

  • Castellini MA, Castellini JM. Defining the limits of diving biochemistry in marine mammals. Comp Biochem Physiol B Biochem Mol Biol. 2004;139(3):509–18.

    Article  PubMed  CAS  Google Scholar 

  • Castellini MA, Rivera PM, Castellini JM. Biochemical aspects of pressure tolerance in marine mammals. Comp Biochem Physiol A Mol Integr Physiol. 2002;133(3):893–9.

    Article  PubMed  Google Scholar 

  • Cavieres G, Alruiz JM, Medina NR, Bogdanovich JM, Bozinovic F. Transgenerational and within-generation plasticity shape thermal performance curves. Ecol Evol. 2019;9(4):2072–82.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chambault P, Albertsen CM, Patterson TA, Hansen RG, Tervo O, Laidre KL, et al. Sea surface temperature predicts the movements of an Arctic cetacean: the bowhead whale. Sci Rep. 2018;8(1):9658.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC. A quantitative review of heterozygosity-fitness correlations in animal populations. Mol Ecol. 2009;18(13):2746–65.

    Article  CAS  PubMed  Google Scholar 

  • Chapman JR, Hellgren O, Helin AS, Kraus RH, Cromie RL, Waldenström J. The evolution of innate immune genes: purifying and balancing selection on β-defensins in waterfowl. Mol Biol Evol. 2016;33(12):3075–87.

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth B, Charlesworth D. The genetic basis of inbreeding depression. Genet Res. 1999;74(3):329–40.

    Article  CAS  PubMed  Google Scholar 

  • Chevin LM, Hoffmann AA. Evolution of phenotypic plasticity in extreme environments. Philos Trans R Soc Lond B Biol Sci. 2017;372(1723):20160138.

    Article  PubMed  PubMed Central  Google Scholar 

  • Clausius E, Mcmahon CR, Hindell MA. Five decades on: use of historical weaning size data reveals that a decrease in maternal foraging success underpins the long-term decline in population of southern elephant seals (Mirounga leonina). PLoS One. 2017;12(3):e0173427.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Coltman DW, Slate J. Microsatellite measures of inbreeding: a meta-analysis. Evolution. 2003;57(5):971–83.

    Article  CAS  PubMed  Google Scholar 

  • Coltman DW, Bowen WD, Wright JM. Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc R Soc B Biol Sci. 1998;265(1398):803–9.

    Article  CAS  Google Scholar 

  • Cooke SJ, Sack L, Franklin CE, Farrell AP, Beardall J, Wikelski M, et al. What is conservation physiology? Perspectives on an increasingly integrated and essential science. Conserv Physiol. 2013;1(1) https://doi.org/10.1093/conphys/cot001.

    Article  PubMed  PubMed Central  Google Scholar 

  • Coria-Galindo E, Rangel-Huerta E, Verdugo-Rodríguez A, Brousset D, Salazar S, Padilla-Noriega L. Rotavirus infections in Galapagos sea lions. J Wildl Dis. 2009;45(3):722–8.

    Article  PubMed  Google Scholar 

  • Cornell LH, Asper ED. Census up-date: captive marine mammals in North America. Int Zoo Yearb. 2007;18:220–4.

    Article  Google Scholar 

  • Costa DP, Sinervo B. Field physiology: physiological insights from animals in nature. Annu Rev Physiol. 2004;66(1):209–38.

    Article  CAS  PubMed  Google Scholar 

  • Côté IM, Darling ES, Brown CJ. Interactions among ecosystem stressors and their importance in conservation. Proc R Soc B Biol Sci. 2016;283(1824):1–9.

    Article  Google Scholar 

  • Dakos V, Matthews B, Hendry A, Levine J, Loeuille N, Norberg J, et al. Ecosystem tipping points in an evolving world. Nat Ecol Evol. 2018;3(3):355–62.

    Article  Google Scholar 

  • Davidson AD, Boyer AG, Kim H, Pompa-Mansilla S, Hamilton MJ, Costa DP, et al. Drivers and hotspots of extinction risk in marine mammals. Proc Natl Acad Sci. 2012;109(9):3395–400.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davidson AD, Shoemaker KT, Weinstein B, Costa GC, Brooks TM, Ceballos G, et al. Geography of current and future global mammal extinction risk. PLoS One. 2017;12(11):e0186934.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Davis M, Faurby S, Svenning J-C. Mammal diversity will take millions of years to recover from the current biodiversity crisis. Proc Natl Acad Sci. 2018;115(44):11262–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denkinger J, Gordillo L, Montero-Serra L, Murillo JC, Guevara N, Hirschfeld M, et al. Urban life of Galapagos sea lions (Zalophus wollebaeki) on San Cristobal Island, Ecuador: colony trends and threats. J Sea Res. 2015;105:10–4.

    Article  Google Scholar 

  • Desforges JP, Levin M, Jasperse L, De Guise S, Eulaers I, Letcher RJ, et al. Effects of polar bear and killer whale derived contaminant cocktails on marine mammal immunity. Environ Sci Technol. 2017;51(19):11431–9.

    Article  CAS  PubMed  Google Scholar 

  • Desforges JP, Hall A, McConnell B, Rosing-Asvid A, Barber JL, Brownlow A, et al. Predicting global killer whale population collapse from PCB pollution. Science. 2018;361(6409):1373–6.

    Article  CAS  PubMed  Google Scholar 

  • Di Guardo G, Centelleghe C, Mazzariol S. Cetacean host-pathogen interaction(s): critical knowledge gaps. Front Immunol. 2018;9:2815.

    Article  PubMed  PubMed Central  Google Scholar 

  • Donelson JM, Salinas S, Munday PL, Shama LNS. Transgenerational plasticity and climate change experiments: where do we go from here? Glob Chang Biol. 2018;24(1):13–34.

    Article  PubMed  Google Scholar 

  • Eirin-Lopez JM, Putnam HM. Marine environmental epigenetics. Ann Rev Mar Sci. 2018;11(1):335–68.

    Article  PubMed  Google Scholar 

  • Elorriaga-Verplancken FR, Sierra-Rodríguez GE, Rosales-Nanduca H, Acevedo-Whitehouse K, Sandoval-Sierra J. 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. PLoS One. 2016;11(5):e0155034.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Espinosa-de Aquino W, Olvera-Ramírez A, Arellano-Carbajal F, Lanz-Mendoza H, Villagrán-Herrera E, Acevedo-Whitehouse K. Protein and RNA extraction from mucosal swabs: a minimally invasive source of ecological data for studies of natural populations. Methods Ecol Evol. 2017;8(3):370–8.

    Article  Google Scholar 

  • Evans TG, Hofmann GE. Defining the limits of physiological plasticity: how gene expression can assess and predict the consequences of ocean change. Philos Trans R Soc Lond B Biol Sci. 2012;367(1596):1733–45.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fareed M, Afzal M. Genetics of consanguinity and inbreeding in health and disease. Ann Hum Biol. 2017;44(2):99–107.

    Article  PubMed  Google Scholar 

  • Flores-Morán A, Banuet-Martínez M, Elorriaga-Verplancken FR, García-Ortuño LE, Sandoval-Sierra J, Acevedo-Whitehouse K. Atypical red blood cells are prevalent in California sea lion pups born during anomalous sea surface temperature events. Physiol Biochem Zool. 2017;90(5):564–74.

    Article  PubMed  Google Scholar 

  • Forcada J, Hoffman JI. Climate change selects for heterozygosity in a declining fur seal population. Nature. 2014;511(7510):462–5.

    Article  CAS  PubMed  Google Scholar 

  • Gibbin EM, Massamba N’Siala G, Chakravarti LJ, Jarrold MD, Calosi P. The evolution of phenotypic plasticity under global change. Sci Rep. 2017;7:17253.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gilbert AT, Fooks AR, Hayman DT, Horton DL, Müller T, Plowright R, et al. Deciphering serology to understand the ecology of infectious diseases in wildlife. Ecohealth. 2013;10(3):298–313.

    Article  PubMed  Google Scholar 

  • Gracey AY, Cossins AR. Application of microarray technology in environmental and comparative physiology. Annu Rev Physiol. 2003;65:231–59.

    Article  CAS  PubMed  Google Scholar 

  • Gui D, Jia K, Xia J, Yang L, Chen J, Wu Y, et al. De novo assembly of the Indo-Pacific humpback dolphin leucocyte transcriptome to identify putative genes involved in the aquatic adaptation and immune response. PLoS One. 2013;8(8):e72417.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, et al. A global map of human impact on marine ecosystems. Science. 2008;319:948–52.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton MJ, Davidson AD, Sibly RM, Brown JH. Universal scaling of production rates across mammalian lineages. Proc R Soc B Biol Sci. 2011;278(1705):560–6.

    Article  Google Scholar 

  • Hamilton CD, Vacquié-Garcia J, Kovacs KM, Ims RA, Kohler J, Lydersen C. Contrasting changes in space use induced by climate change in two Arctic marine mammal species. Biol Lett. 2019;15(3):20180834.

    Article  PubMed  PubMed Central  Google Scholar 

  • Herman JJ, Spencer HG, Donohue K, Sultan SE. How stable “should” epigenetic modifications be? Insights from adaptive plasticity and bet hedging. Evolution. 2014;68(3):632–43.

    Article  PubMed  Google Scholar 

  • Hoegh-Guldberg O, Bruno JF. The impact of climate change on the world’s marine ecosystems. Science. 2010;328:1523–9.

    Article  CAS  PubMed  Google Scholar 

  • Hoelzel AR, Natoli A, Dahlheim ME, Olavarria C, Baird RW, Black NA. Low worldwide genetic diversity in the killer whale (Orcinus orca): implications for demographic history. Proc R Soc B Biol Sci. 2002;269(1499):1467–73.

    Article  Google Scholar 

  • Hoffman JI, Boyd JANL, Amosl W. Exploring the relationship between parental relatedness and male reproductive success in the Antarctic fur seal Arctocephalus gazelle. Evolution. 2004;58(9):2087–99.

    Article  PubMed  Google Scholar 

  • Hoffmann AA, Willi Y. Detecting genetic responses to environmental change. Nat Rev Genet. 2008;9(6):421–32.

    Article  CAS  PubMed  Google Scholar 

  • Hofmann GE, Todgham AE. Living in the now: physiological mechanisms to tolerate a rapidly changing environment. Annu Rev Physiol. 2010;72(1):127–45.

    Article  CAS  PubMed  Google Scholar 

  • Holt WV, Brown JL, Comizzoli P. Reproductive sciences in animal conservation. Adv Exp Med Biol. 2014;753:3–14.

    Article  PubMed  Google Scholar 

  • Hunt KE, Moore MJ, Rolland RM, Kellar NM, Hall AJ, Kershaw J, et al. Overcoming the challenges of studying conservation physiology in large whales: a review of available methods. Conserv Physiol. 2013;1(1):cot006.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hunt KE, Stimmelmayr R, George C, Hanns C, Suydam R, Brower H, et al. Baleen hormones: a novel tool for retrospective assessment of stress and reproduction in bowhead whales (Balaena mysticetus). Conserv Physiol. 2014;2(1):cou030.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hunt KE, Rolland RM, Kraus SD. Conservation physiology of an uncatchable animal: the North Atlantic right whale (Eubalaena glacialis). Integr Comp Biol. 2015;55(4):577–86.

    Article  PubMed  Google Scholar 

  • James TY, Toledo LF, Rödder D, da Silva Leite D, Belasen AM, Betancourt-Román CM, et al. Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecol Evol. 2015;5(18):4079–97.

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaramillo-Legorreta A, Cardenas-Hinojosa G, Nieto-Garcia E, Rojas-Bracho L, Ver Hoef J, Moore J, et al. Passive acoustic monitoring of the decline of Mexico’s critically endangered vaquita. Conserv Biol. 2016;31(1):183–91.

    Article  PubMed  Google Scholar 

  • Johnstone CP, Lill A, Reina RD. Use of erythrocyte indicators of health and condition in vertebrate ecophysiology: a review and appraisal. Biol Rev Camb Philos Soc. 2017;92(1):150–68.

    Article  PubMed  Google Scholar 

  • Juárez-Ruiz A, Elorriaga-Verplancken FR, Moreno-Sánchez XG, Aguíniga-García S, Amador-Capitanachi MJ, Gálvez C. Diversification of foraging habits among Guadalupe fur seals from their only well-established breeding colony, Guadalupe Island, Mexico. Mar Biol. 2018;165:86.

    Article  Google Scholar 

  • Kershaw JL, Botting CH, Brownlow A, Hall AJ. Not just fat: investigating the proteome of cetacean blubber tissue. Conserv Physiol. 2018;6(1):coy003.

    Article  PubMed  PubMed Central  Google Scholar 

  • Keyghobadi N. The genetic implications of habitat fragmentation for animals. Can J Zool. 2007;85(10):1049–64.

    Article  Google Scholar 

  • Khudyakov JI, Preeyanon L, Champagne CD, Ortiz RM, Crocker DE. Transcriptome analysis of northern elephant seal (Mirounga angustirostris) muscle tissue provides a novel molecular resource and physiological insights. BMC Genomics. 2015;16:64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kilikevicius A, Venckunas T, Zelniene R, Carroll AM, Lionikaite S, Ratkevicius A, et al. Divergent physiological characteristics and responses to endurance training among inbred mouse strains. Scand J Med Sci Sports. 2013;23(5):657–68.

    CAS  PubMed  Google Scholar 

  • Kirschman LJ, McCue MD, Boyles JG, Warne RW. Exogenous stress hormones alter energetic and nutrient costs of development and metamorphosis. J Exp Biol. 2017a;220(18):3391–7.

    Article  PubMed  Google Scholar 

  • Kirschman LJ, Crespi EJ, Warne RW. Critical disease windows shaped by stress exposure alter allocation trade-offs between development and immunity. J Anim Ecol. 2017b;87(1):235–46.

    Article  PubMed  Google Scholar 

  • Kleiman DG. Reintroduction programs. In: Wild mammals in captivity. Chicago: University of Chicago Press; 1996. p. 297–305.

    Google Scholar 

  • Kloch A, Wenzel MA, Laetsch DR, Michalski O, Welc-Falȩciak R, Piertney SB. Signatures of balancing selection in toll-like receptor (TLRs) genes—novel insights from a free-living rodent. Sci Rep. 2018;8(1):8361.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kretzmann M, Mentzer L, DiGiovanni R, Leslie MS, Amato G. Microsatellite diversity and fitness in stranded juvenile harp seals (Phoca groenlandica). J Hered. 2006;97(6):555–60.

    Article  CAS  PubMed  Google Scholar 

  • Kuhn CE, Costa DP. Interannual variation in the at-sea behavior of California sea lions (Zalophus californianus). Mar Mamm Sci. 2014;30:1297–319.

    Article  Google Scholar 

  • Laidre KL, Stern H, Kovacs KM, Lowry L, Moore SE, Regehr EV, et al. Arctic marine mammal population status, sea ice habitat loss, and conservation recommendations for the 21st century. Conserv Biol. 2015;29(3):724–37.

    Article  PubMed  PubMed Central  Google Scholar 

  • Le Quesne WJF, Pinnegar JK. The potential impacts of ocean acidification: scaling from physiology to fisheries. Fish Fish. 2012;12:333–44.

    Article  Google Scholar 

  • Leaper R, Cooke J, Trathan P, Reid K, Rowntree V, Payne R. Global climate drives southern right whale (Eubalaena australis) population dynamics. Biol Lett. 2006;2(2):289–92.

    Article  PubMed  PubMed Central  Google Scholar 

  • Leroy G, Carroll EL, Bruford MW, DeWoody JA, Strand A, Waits L, et al. Next-generation metrics for monitoring genetic erosion within populations of conservation concern. Evol Appl. 2017;11(7):1066–83.

    Article  PubMed  PubMed Central  Google Scholar 

  • Letcher RJ, Bustnes JO, Dietz R, Jenssen BM, Jørgensen EH, Sonne C, et al. Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci Total Environ. 2010;408(15):2995–3043.

    Article  CAS  PubMed  Google Scholar 

  • Lotze HK, Coll M, Magera AM, Ward-Paige C, Airoldi L. Recovery of marine animal populations and ecosystems. Trends Ecol Evol. 2011;26(11):595–605.

    Article  PubMed  Google Scholar 

  • Luo Z, Jiang Z, Tang S. Impacts of climate change on distributions and diversity of ungulates on the Tibetan Plateau. Ecol Appl. 2015;25(1):24–38.

    Article  PubMed  Google Scholar 

  • Lurie IW, Prytkov A, Meldere L. Meckel syndrome in different populations. Am J Med Genet. 1984;18(4):661–9.

    Article  CAS  PubMed  Google Scholar 

  • Machalaba CM, Karesh WB. Emerging infectious disease risk: shared drivers with environmental change. Rev Sci Tech. 2018;36(2):435–44.

    Article  Google Scholar 

  • Madliger CL, Love OP, Hultine KR, Cooke SJ. The conservation physiology toolbox: status and opportunities. Conserv Physiol. 2018;6(1):coy029.

    PubMed  PubMed Central  Google Scholar 

  • Matesanz S, Gianoli E, Valladares F. Global change and the evolution of phenotypic plasticity in plants. Ann N Y Acad Sci. 2010;1206:35–55.

    Article  PubMed  Google Scholar 

  • McDonald PJ, Nano CEM, Ward SJ, Stewart A, Pavey CR, Luck GW, et al. Habitat as a mediator of mesopredator-driven mammal extinction. Conserv Biol. 2017;31(5):1183–91.

    Article  PubMed  Google Scholar 

  • McMahon CR, Harcourt RG, Burton HR, Daniel O, Hindell MA. Seal mothers expend more on offspring under favourable conditions and less when resources are limited. J Anim Ecol. 2017;86(2):359–70.

    Article  PubMed  Google Scholar 

  • McNew L. The nature, origin, and evolution of parasitism. In: Horsfall JG, Dimond AE, editors. Plant pathology—an advanced treatise. New York: Academic Press; 1960. p. 19–69.

    Google Scholar 

  • Metcalfe JD, le Quesne WJF, Cheung WWL, Righton DA. Conservation physiology for applied management of marine fish: an overview with perspectives on the role and value of telemetry. Philos Trans R Soc Lond B Biol Sci. 2012;367(1596):1746–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miles AK, Bowen L, Ballachey B, Bodkin JL, Murray M, Estes JL, et al. Variations of transcript profiles between sea otters Enhydra lutris from Prince William Sound, Alaska, and clinically normal reference otters. Mar Ecol Prog Ser. 2012;451:201–12.

    Article  Google Scholar 

  • Monaco CJ, Helmuth B. Tipping points, thresholds and the keystone role of physiology in marine climate change research. Adv Mar Biol. 2011;60:123–60.

    Article  PubMed  Google Scholar 

  • Monteiro WP, Veiga JC, Silva AR, Carvalho C d S, Lanes ÉCM, Rico Y, et al. Everything you always wanted to know about gene flow in tropical landscapes (but were afraid to ask). PeerJ. 2019;7:e6446.

    Article  PubMed  PubMed Central  Google Scholar 

  • Moore SE. Marine mammals as ecosystem sentinels. J Mammal. 2008;89(3):534–40.

    Article  Google Scholar 

  • Morell V. Conservation biology: can the vaquita be saved? Science. 2008;321(5890):767.

    Article  CAS  PubMed  Google Scholar 

  • Morey JS, Neely MG, Lunardi D, Anderson PE, Schwacke LH, Campbell M, et al. RNA-Seq analysis of seasonal and individual variation in blood transcriptomes of healthy managed bottlenose dolphins. BMC Genomics. 2016;17:720.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moritz C, Agudo R. The future of species under climate. Science. 2013;341(6154):504–8.

    Article  CAS  PubMed  Google Scholar 

  • Morueta-Holme N, Fløjgaard C, Svenning JC. Climate change risks and conservation implications for a threatened small-range mammal species. PLoS One. 2010;5(4):e10360.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moura AE, Kenny JG, Chaudhuri R, Hughes MA, Welch A J, Reisinger RR, et al. Population genomics of the killer whale indicates ecotype evolution in sympatry involving both selection and drift. Mol Ecol. 2014;23(21):5179–92.

    Article  PubMed  PubMed Central  Google Scholar 

  • Muletz-Wolz CR, Barnett SE, DiRenzo GV, Zamudio KR, Toledo LF, James TY, et al. Diverse genotypes of the amphibian-killing fungus produce distinct phenotypes through plastic responses to temperature. J Evol Biol. 2019; https://doi.org/10.1111/jeb.13413.

    Article  PubMed  Google Scholar 

  • Neely MG, Morey JS, Anderson P, Balmer BC, Ylitalo GM, Zolman ES, et al. Skin transcriptomes of common bottlenose dolphins (Tursiops truncatus) from the northern Gulf of Mexico and southeastern U.S. Atlantic coasts. Mar Genomics. 2018;38:45–58.

    Article  PubMed  Google Scholar 

  • NOAA. Centers for Environmental Information, State of the Climate: global climate report for annual 2017; 2017. Published online Jan 2018; Accessed 19 Dec 2018.

    Google Scholar 

  • Nussey DH, Wilson AJ, Brommer JE. The evolutionary ecology of individual phenotypic plasticity in wild populations. J Evol Biol. 2007;20(3):831–44.

    Article  CAS  PubMed  Google Scholar 

  • O’Brien SJ, Evermann JF. Interactive influence of infectious disease and genetic diversity in natural populations. Trends Ecol Evol. 1988;3(10):254–9.

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Corry-Crowe G. Climate change and the molecular ecology of Arctic marine mammals. Ecol Appl. 2008;18(2):S56–76.

    Article  PubMed  Google Scholar 

  • Oostra V, Saastamoinen M, Zwaan BJ, Wheat CW. Strong phenotypic plasticity limits potential for evolutionary responses to climate change. Nat Commun. 2018;9(1):1005.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Parente CL, Araújo JP, Araújo ME. Diversity of cetaceans as tool in monitoring environmental impacts of seismic surveys. Biota Neotrop. 2007;7(1):49–56.

    Article  Google Scholar 

  • Pauls SU, Nowak C, Bálint M, Pfenninger M. The impact of global climate change on genetic diversity within populations and species. Mol Ecol. 2013;22(4):925–46.

    Article  PubMed  Google Scholar 

  • Peñín I, Figueroa-Cabañas ME, Guerrero-de la Rosa F, Soto-García LA, Álvarez-Martínez R, Flores-Morán A, et al. Transcriptional profiles of California sea lion peripheral NK and CD+8 T cells reflect ecological regionalization and infection by oncogenic viruses. Front Immunol. 2019;10:413.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Piersma T, Drent J. Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol. 2003;18(5):228–33.

    Article  Google Scholar 

  • Pomeroy P. Reproductive cycles of marine mammals. Anim Reprod Sci. 2011;124(3–4):184–93.

    Article  CAS  PubMed  Google Scholar 

  • Ratajczak Z, Carpenter SR, Ives AR, Kucharik CJ, Ramiadantsoa T, Stegner MA, et al. Abrupt change in ecological systems: inference and diagnosis. Trends Ecol Evol. 2018;33(7):513–26.

    Article  PubMed  Google Scholar 

  • Redding DW, Mooers AO. Ranking mammal species for conservation and the loss of both phylogenetic and trait diversity. PLoS One. 2015;10(12):e0141435.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Regehr EV, Laidre KL, Akcakaya HR, Amstrup SC, Atwood TC, Lunn NJ, et al. Conservation status of polar bears (Ursus maritimus) in relation to projected sea-ice declines. Biol Lett. 2016;12(12):20160556.

    Article  PubMed  PubMed Central  Google Scholar 

  • Relyea RA. Costs of phenotypic plasticity. Am Nat. 2017;159(3):272.

    Article  Google Scholar 

  • Richard JT, Robeck TR, Osborn SD, Naples L, McDermott A, LaForge R, et al. Testosterone and progesterone concentrations in blow samples are biologically relevant in belugas (Delphinapterus leucas). Gen Comp Endocrinol. 2017;246:183–93.

    Article  CAS  PubMed  Google Scholar 

  • Rijks JM, Hoffman JI, Kuiken T, Osterhaus ADME, Amos W. Heterozygosity and lungworm burden in harbour seals (Phoca vitulina). Heredity. 2008;100(6):587–93.

    Article  CAS  PubMed  Google Scholar 

  • Robeck TR, Nollens HH. Hematological and serum biochemical analytes reflect physiological challenges during gestation and lactation in killer whales (Orcinus orca). Zoo Biol. 2013;32(5):497–509.

    Article  CAS  PubMed  Google Scholar 

  • Rode KD, Regehr EV, Douglas DC, Durner G, Derocher AE, Thiemann GW, et al. Variation in the response of an Arctic top predator experiencing habitat loss: feeding and reproductive ecology of two polar bear populations. Glob Chang Biol. 2014;20(1):76–88.

    Article  PubMed  Google Scholar 

  • Rode KD, Wilson RR, Regehr EV, St Martin M, Douglas DC, Olson J. Increased land use by Chukchi Sea polar bears in relation to changing sea ice conditions. PLoS One. 2015;10(11):e0142213.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roff DA. Life history evolution. Oxford: Oxford University Press; 2001.

    Google Scholar 

  • Sánchez-Lugo A, Morice C, Berrisford P, Argüez A. Temperature [in state of the climate in 2017]. Bull Am Meteorol Soc. 2018;99(8):S11–3.

    Google Scholar 

  • Sandom C, Faurby S, Sandel B, Svenning J-C. Global late quaternary megafauna extinctions linked to humans, not climate change. Proc R Soc B Biol Sci. 2014;281(1787):20133254.

    Article  Google Scholar 

  • Santini L, González-Suárez M, Russo D, Gonzalez-Voyer A, von Hardenberg A, Ancillotto L. One strategy does not fit all: determinants of urban adaptation in mammals. Ecol Lett. 2019;22(2):365–76.

    Article  PubMed  Google Scholar 

  • Schnitzler JG, Reckendorf A, Pinzone M, Autenrieth M, Tiedemann R, Covaci A, et al. Supporting evidence for PCB pollution threatening global killer whale population. Aquat Toxicol. 2018;206:102–4.

    Article  PubMed  CAS  Google Scholar 

  • Scholthof KB. The disease triangle: pathogens, the environment and society. Nat Rev Microbiol. 2007;5(2):152–6.

    Article  CAS  PubMed  Google Scholar 

  • Seebacher F, Franklin CE. Determining environmental causes of biological effects: the need for a mechanistic physiological dimension in conservation biology. Philos Trans R Soc Lond B Biol Sci. 2012;367(1596):1607–14.

    Article  PubMed  PubMed Central  Google Scholar 

  • Seguel M, Montalva F, Perez-Venegas D, Gutiérrez J, Paves HJ, Müller A, et al. Immune-mediated hookworm clearance and survival of a marine mammal decrease with warmer ocean temperatures. Elife. 2018;7:e38432.

    Article  PubMed  PubMed Central  Google Scholar 

  • Seyboth E, Groch KR, Dalla Rosa L, Reid K, Flores PA, Secchi ER. Southern right whale (Eubalaena australis) reproductive success is influenced by krill (Euphausia superba) density and climate. Sci Rep. 2016;6:28205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sitt T, Bowen L, Lee CS, Blanchard MT, McBain J, Dold C, Stott JL. Longitudinal evaluation of leukocyte transcripts in killer whales (Orcinus Orca). Vet Immunol Immunopathol. 2016;175:7–15. https://doi.org/10.1016/j.vetimm.2016.04.011.

    Article  CAS  PubMed  Google Scholar 

  • Snell-Rood E, Cothran R, Espeset A, Jeyasingh P, Hobbie S, Morehouse NI. Life-history evolution in the anthropocene: effects of increasing nutrients on traits and trade-offs. Evol Appl. 2015;8(7):635–49.

    Article  PubMed  PubMed Central  Google Scholar 

  • Somero GN. Comparative physiology: a “crystal ball” for predicting consequences of global change. Am J Physiol Regul Integr Comp Physiol. 2011;301:R1–14.

    Article  CAS  PubMed  Google Scholar 

  • Stearns SC. The evolution of life histories. Oxford: Oxford University Press; 1992.

    Google Scholar 

  • Stoffel MA, Humble E, Paijmans AJ, Acevedo-Whitehouse K, Chilvers BL, Dickerson B, et al. Demographic histories and genetic diversity across pinnipeds are shaped by human exploitation, ecology and life-history. Nat Commun. 2018;9(1):4836.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutton JT, Nakagawa S, Robertson BC, Jamieson IG. Disentangling the roles of natural selection and genetic drift in shaping variation at MHC immunity genes. Mol Ecol. 2011;20(21):4408–20.

    Article  PubMed  Google Scholar 

  • Szpak P, Buckley M, Darwent CM, Richards MP. Long-term ecological changes in marine mammals driven by recent warming in northwestern Alaska. Glob Chang Biol. 2018;24(1):490–503.

    Article  PubMed  Google Scholar 

  • Thomas MA, Klaper R. Genomics for the ecological toolbox. Trends Ecol Evol. 2004;19(8):439–45.

    Article  PubMed  Google Scholar 

  • Thompson LA, Spoon TR, Goertz CEC, Hobbs RC, Romano TA. Blow collection as a non-invasive method for measuring cortisol in the beluga (Delphinapterus leucas). PLoS One. 2014;9(12):e114062.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tulloch VJD, Plagányi ÉE, Brown C, Richardson AJ, Matear R. Future recovery of baleen whales is imperiled by climate change. Glob Chang Biol. 2019;25(4):1263–81.

    Article  PubMed Central  Google Scholar 

  • Urban MC, Bocedi G, Hendry AP, Mihoub JB, Pe’er G, Singer A, et al. Improving the forecast for biodiversity under climate change. Science. 2016;353(6304):aad8466.

    Article  PubMed  CAS  Google Scholar 

  • Valsecchi E, Amos W, Raga JA, Podesta M, Sherwin W. The effects of inbreeding on mortality during a morbillivirus outbreak in the Mediterranean striped dolphin (Stenella coeruleoalba). Anim Conserv. 2004;7(2004):139–46.

    Article  Google Scholar 

  • Van Bressem MF, Raga JA, Di Guardo G, Jepson PD, Duignan PJ, Siebert U, et al. Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Dis Aquat Organ. 2009;86(2):143–57.

    Article  PubMed  Google Scholar 

  • Van Bressem M, Duignan P, Banyard A, Barbieri M, Colegrove K, De Guise S, et al. Cetacean morbillivirus: current knowledge and future directions. Viruses. 2014;6(12):5145–81.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Dolah FM, Neely MG, McGeorge LE, Balmer BC, Ylitalo GM, Zolman ES, et al. Seasonal variation in the skin transcriptome of common bottlenose dolphins (Tursiops truncatus) from the northern Gulf of Mexico. PLoS One. 2015;10(6):e0130934.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Venesky MD, Mendelson JR, Sears BF, Stiling P, Rohr JR. Selecting for tolerance against pathogens and herbivores to enhance success of reintroduction and translocation. Conserv Biol. 2012;26(4):586–92.

    Article  PubMed  Google Scholar 

  • Warne RW, Kirschman L, Zeglin L. Manipulation of gut microbiota during critical developmental windows affect host physiological performance and disease susceptibility across ontogeny. J Anim Ecol. 2019; https://doi.org/10.1111/1365-2656.12973.

  • Weber DS, Stewart BS, Lehman N. Genetic consequences of a severe population bottleneck in the Guadalupe fur seal (Arctocephalus townsendi). J Hered. 2004;95(2):144–53.

    Article  CAS  PubMed  Google Scholar 

  • Wensveen PJ, Isojunno S, Hansen RR, Von Benda-Beckmann AM, Kleivane L, Van Ijsselmuide S, et al. Northern bottlenose whales in a pristine environment respond strongly to close and distant navy sonar signals. Proc R Soc B Biol Sci. 2019;286:20182592.

    Article  Google Scholar 

  • Whiteman JP, Harlow HJ, Durner GM, Regehr EV, Amstrup SC, Ben-David M. Heightened immune system function in polar bears using terrestrial habitats. Physiol Biochem Zool. 2018;92(1):1–11.

    Article  Google Scholar 

  • Wiig Ø, Aars J, Born EW. Effects of climate change on polar bears. Sci Prog. 2008;91(2):151–73.

    Article  PubMed  Google Scholar 

  • Wikelski M, Cooke SJ. Conservation physiology. Trends Ecol Evol. 2006;21:38–46.

    Article  PubMed  Google Scholar 

  • Wood CL. Environmental change and the ecology of infectious disease. Science. 2014;346(6214):1192.

    Article  PubMed  Google Scholar 

  • Worm B, Barbier EB, Beaumont N, Duffy JE, Folke C, Halpern BS, et al. Impacts of biodiversity loss on ocean ecosystem services. Science. 2006;314(5800):787–90.

    Article  CAS  PubMed  Google Scholar 

  • Younger JL, Emmerson LM, Miller KJ. The influence of historical climate changes on Southern Ocean marine predator populations: a comparative analysis. Glob Chang Biol. 2016;22(2):474–93.

    Article  PubMed  Google Scholar 

  • Zera AJ, Harshman LG. The physiology of life history trade-offs in animals. Annu Rev Ecol Syst. 2001;32:95–126.

    Article  Google Scholar 

Download references

Acknowledgments

Fernando Elorriaga-Verplancken and Lizabeth Bowen kindly reviewed this chapter and made insightful comments, all of which were incorporated in the final version. The author is funded by CONACYT Ciencia Básica Program CB 2017–2018 (Research Grant A1-S-16417). The funding organization had no role in the topic, decision to publish, or preparation of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Karina Acevedo-Whitehouse .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Acevedo-Whitehouse, K. (2019). Physiological Thresholds in the Context of Marine Mammal Conservation. In: Comizzoli, P., Brown, J., Holt, W. (eds) Reproductive Sciences in Animal Conservation. Advances in Experimental Medicine and Biology, vol 1200. Springer, Cham. https://doi.org/10.1007/978-3-030-23633-5_6

Download citation

Publish with us

Policies and ethics