Metabolic cost of the activation of immune response in the fish-eating myotis (Myotis vivesi): The effects of inflammation and the acute phase response

PLoS ONE

Volumn 11, Issue 10, 2016, Pages

  Aída, Otálora Ardila ^a   Herrera, M L ^a   Flores Martínez, José Juan ^a   Welch, Kenneth C ^b  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

LIPOPOLYSACCHARIDE; PHYTOHEMAGGLUTININ;

ACUTE PHASE RESPONSE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY MASS; CONTROLLED STUDY; FEMALE; FISH EATING MYOTIS; IMMUNE RESPONSE; INFECTION; INFLAMMATION; MALE; METABOLISM; MYOTIS; MYOTIS VIVESI; NONHUMAN; RESTING METABOLIC RATE; SKIN SWELLING; SKIN TEMPERATURE; TEMPERATURE MEASUREMENT; ANIMAL; BASAL METABOLIC RATE; BAT; BODY TEMPERATURE; DRUG EFFECTS; ENERGY METABOLISM; IMMUNOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACUTE-PHASE REACTION; ANIMALS; BASAL METABOLISM; BODY TEMPERATURE; CHIROPTERA; ENERGY METABOLISM; FEMALE; INFLAMMATION; LIPOPOLYSACCHARIDES; MALE; PHYTOHEMAGGLUTININS;

EID: 84994036902     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0164938     Document Type: Article

References (51)

1. Owen-Ashley NT, Wingfield JC. Acute phase responses of passerine birds: characterization and seasonal variation. J Ornithol. 2007; 148: 583-591. doi: 10.1007/s10336-007-0197-2
2. Viljoen H, Bennett NC, Lutermann H. Life-history traits, but not season, affect the febrile response to a lipopolysaccharide challenge in highveld mole-rats. J Zool. 2011; 285: 222-229. doi: 10.1111/j.1469-7998.2011.00833.x
3. Barton GM. A calculated response: control of inflammation by the innate immune system. J Clin Invest. 2008; 118: 413-420. doi: 10.1172/JCI34431 PMID: 18246191
4. Baumann H, Gauldie J. The acute phase response. Immunol Today. 1994; 15: 74-80. doi: 10.1016/ 0167-5699(94)90137-6 PMID: 7512342
5. Lochmiller RL, Deerenberg C. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos. 2000; 88: 87-98.
6. Klasing K. The cost of immunity. Curr Zool. 2004; 50: 961-969.
7. Buehler DM, Tieleman BI, Piersma T. How do migratory species stay healthy over the annual cycle? A conceptual model for immune function and for resistance to disease. Integr Comp Biol. 2010; 50: 346-357. doi: 10.1093/icb/icq055 PMID: 21558209
8. Sheldon BC, Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol. 1996; 11: 317-321. PMID: 21237861
9. Hasselquist D, Nilsson J-Å. Physiological mechanisms mediating costs of immune responses: what can we learn from studies of birds? Anim Behav. 2012; 83: 1303-1312. doi: 10.1016/j.anbehav.2012. 03.025
10. Kennedy M, Nager R. The perils and prospects of using phytohaemagglutinin in evolutionary ecology. Trends Ecol Evol. 2006; 21: 653-655. doi: 10.1016/j.tree.2006.09.017 PMID: 17028055
11. Boughton RK, Joop G, Armitage SAO. Outdoor immunology: methodological considerations for ecologists: advancing ecological immunology methods. Funct Ecol. 2011; 25: 81-100. doi: 10.1111/j.1365-2435.2010.01817.x
12. Demas G, Greives T, Chester E, French S. The energetics of immunity: mechanisms of trade-off in immunology. In: Demas G., Nelson R., editors. Ecoimmunology. Oxford: Oxford University Press; 2011. pp. 259-296.
13. Bonneaud C, Mazuc J, Gonzalez G, Haussy C, Chastel O, Faivre B, et al. Assessing the cost of mounting an immune response. Am Nat. 2003; 161: 367-379. doi: 10.1086/346134 PMID: 12703483
14. Canale CI, Henry P-Y. Energetic costs of the immune response and torpor use in a primate. Funct Ecol. 2011; 25: 557-565. doi: 10.1111/j.1365-2435.2010.01815.x
15. Martin LB, Scheuerlein A, Wikelski M. Immune activity elevates energy expenditure of house sparrows: a link between direct and indirect costs? Proc R Soc B Biol Sci. 2003; 270: 153-158. doi: 10.1098/ rspb.2002.2185 PMID: 12590753
16. Nilsson J-Å, Granbom M, Råberg L. Does the strength of an immune response reflect its energetic cost? J Avian Biol. 2007; 38: 488-494. doi: 10.1111/j.2007.0908-8857.03919.x
17. Derting TL, Compton S. Immune response, not immune maintenance, is energetically costly in wild white-footed mice (Peromyscus leucopus). Physiol Biochem Zool. 2003; 76: 744-752. doi: 10.1086/ 375662 PMID: 14671721
18. Lee KA, Martin LB, Wikelski MC. Responding to inflammatory challenges is less costly for a successful avian invader, the house sparrow (Passer domesticus), than its less-invasive congener. Oecologia. 2005; 145: 243-250. doi: 10.1007/s00442-005-0113-5 PMID: 15965757
19. Zhiquiang Z, Fengtong Q, Dehua W. Sex and seasonal differences and energetic cost of phytohemagglutinin responses in wild Mongolian gerbils (Meriones unguiculatus). Acta Theriol Sin. 2011; 3: 284-290.
20. Merlo JL, Cutrera AP, Luna F, Zenuto RR. PHA-induced inflammation is not energetically costly in the subterranean rodent Ctenomys talarum (tuco-tucos). Comp Biochem Physiol A Mol Integr Physiol. 2014; 175: 90-95. doi: 10.1016/j.cbpa.2014.05.021 PMID: 24905647
21. Rodríguez A, Broggi J, Alcaide M, Negro JJ, Figuerola J. Determinants and short-term physiological consequences of PHA immune response in lesser kestrel nestlings. J Exp Zool Part Ecol Genet Physiol. 2014; 321: 376-386. doi: 10.1002/jez.1868 PMID: 24807828
22. Marais M, Maloney SK, Gray DA. The metabolic cost of fever in Pekin ducks. J Therm Biol. 2011; 36: 116-120. doi: 10.1016/j.jtherbio.2010.12.004
23. King MO, Swanson DL. Activation of the immune system incurs energetic costs but has no effect on the thermogenic performance of house sparrows during acute cold challenge. J Exp Biol. 2013; 216: 2097-2102. doi: 10.1242/jeb.079574 PMID: 23430994
24. Burness G, Armstrong C, Fee T, Tilman-Schindel E. Is there an energetic-based trade-off between thermoregulation and the acute phase response in zebra finches? J Exp Biol. 2010; 213: 1386-1394. doi: 10.1242/jeb.027011 PMID: 20348351
25. MacDonald L, Begg D, Weisinger RS, Kent S. Calorie restricted rats do not increase metabolic rate post-LPS, but do seek out warmer ambient temperatures to behaviourally induce a fever. Physiol Behav. 2012; 107: 762-772. doi: 10.1016/j.physbeh.2012.06.009 PMID: 22722100
26. Hegemann A, Matson KD, Versteegh MA, Tieleman BI. Wild skylarks seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle. Powell J, editor. PLoS ONE. 2012; 7: e36358. doi: 10.1371/journal.pone.0036358 PMID: 22570706
27. Baze MM, Hunter K, Hayes JP. Chronic hypoxia stimulates an enhanced response to immune challenge without evidence of an energetic tradeoff. J Exp Biol. 2011; 214: 3255-3268. doi: 10.1242/jeb. 054544 PMID: 21900473
28. Sköld-Chiriac S, Nord A, Nilsson J-Å, Hasselquist D. Physiological and behavioral responses to an acute-phase response in zebra finches: immediate and short-term effects. Physiol Biochem Zool. 2014; 87: 288-298. doi: 10.1086/674789 PMID: 24642546
29. Banet M. Fever and survival in the rat. Metabolic versus temperature response. Experientia. 1981; 37: 1302-1304. PMID: 7327237
30. Kluger MJ. Is fever beneficial? Yale J Biol Med. 1986; 59: 89. PMID: 3488621
31. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T. Bats: important reservoir hosts of emerging viruses. Clin Microbiol Rev. 2006; 19: 531-545. doi: 10.1128/CMR.00017-06 PMID: 16847084
32. Luis AD, Hayman DTS, O'Shea TJ, Cryan PM, Gilbert AT, Pulliam JRC, et al. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc R Soc B Biol Sci. 2013; 280: 20122753-20122753. doi: 10.1098/rspb.2012.2753 PMID: 23378666
33. Mühldorfer K. Bats and bacterial pathogens: a review. Zoonoses Public Health, 2013; 60: 93-103. doi: 10.1111/j.1863-2378.2012.01536.x PMID: 22862791
34. Brook CE, Dobson AP. Bats as 'special'reservoirs for emerging zoonotic pathogens. Trends Microbiol. 2015; 23: 172-180. doi: 10.1016/j.tim.2014.12.004 PMID: 25572882
35. Christe P, Arlettaz R, Vogel P. Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecol Lett. 2000; 3: 207-212.
36. Allen LC, Turmelle AS, Mendonça MT, Navara KJ, Kunz TH, McCracken GF. Roosting ecology and variation in adaptive and innate immune system function in the Brazilian free-tailed bat (Tadarida brasiliensis). J Comp Physiol B. 2009; 179: 315-323. doi: 10.1007/s00360-008-0315-3 PMID: 19002470
37. Schneeberger K, Czirjak GA, Voigt CC. Inflammatory challenge increases measures of oxidative stress in a free-ranging, long-lived mammal. J Exp Biol. 2013; 216: 4514-4519. doi: 10.1242/jeb. 090837 PMID: 24031067
38. Stockmaier S, Dechmann DKN, Page RA, O'Mara MT. No fever and leucocytosis in response to a lipopolysaccharide challenge in an insectivorous bat. Biol Lett. 2015; 11: 20150576. doi: 10.1098/rsbl. 2015.0576 PMID: 26333664
39. Flores-Martinez JJ, Floyd CH, Herrera M. LG, May B. Genetic variation and population size of the endangered fishing bat, Myotis vivesi, in Isla Partida. In: Sánchez-Cordero V, Medellín R, editors. Contribuciones mastozoológicas en homenaje a Bernardo Villa. México: Universidad Nacional Autónoma de México, Comisión Nacional para el Conocimiento y Uso de la Biodiversidad; 2005. pp. 187-192.
40. Barclay RMR, Kalcounis MC, Crampton LH, Stefan C, Vonhof MJ, Wilkinson L, et al. Can external radiotransmitters be used to assess body temperature and torpor in bats? J Mammal. 1996; 77: 1102-1106.
41. Williams JB, Tieleman BI, Shobrak M. Validation of temperature-sensitive radio transmitters for measurement of body temperature in small animals. Ardea. 2009; 97: 120-124. doi: 10.5253/078.097. 0115
42. Lighton JRB. Measuring metabolic rates: a manual for scientists. Oxford; New York: Oxford University Press; 2008.
43. Welch K Jr, Otálora-Ardila A, Herrera M LG, Flores-Martínez JJ. The cost of digestion in the fish-eating myotis (Myotis vivesi). J Exp Biol. 2015; 218: 1180-1187. doi: 10.1242/jeb.115964 PMID: 25911733
44. Zeileis A, Grothendieck G. zoo: S3 Infrastructure for regular and irregular time series. J Stat Softw. 2005; 14: 1-27.
45. R Core Team. R: A Language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013.
46. StatSoft, Inc. Statistica. Version 7 [computer program]. StatSoft, Inc., Tulsa, Okla. 2004.
47. Boughton RK, Bridge ES, Schoech SJ. Energetic trade-offs between immunity and reproduction in male japanese quail (Coturnix coturnix). J Exp Zool Part A Ecol Genet Physiol. 2007; 307A: 479-487. doi: 10.1002/jez.402 PMID: 17647272
48. Previtali MA, Ostfeld RS, Keesing F, Jolles AE, Hanselmann R, Martin LB. Relationship between pace of life and immune responses in wild rodents. Oikos 2012; 121: 1483-1492.
49. Speakman JR, Król E. Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J Anim Ecol. 2010; 79: 726-746. doi: 10.1111/j.1365-2656.2010.01689. x PMID: 20443992
50. Carpenter RE. Salt and water metabolism in the marine fish-eating bat Pizonyx vivesi. Comp Biochem Physiol 1968; 24: 951-964.51. PMID: 5650499
51. Giorgi MS, Arlettaz R, Christe P, Vogel P. The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis). Proc R Soc B Biol Sci. 2001; 268: 2071-2075. doi: 10.1098/rspb.2001.1686 PMID: 11571055