Mammal Research

, Volume 63, Issue 4, pp 397–404 | Cite as

Metabolic cost of acute phase response in the frugivorous bat, Artibeus lituratus

  • Adriana L. Guerrero-Chacón
  • David Rivera-Ruíz
  • Vladimir Rojas-Díaz
  • Camila Triana-Llanos
  • Andrea Niño-Castro
Original Paper


Bats play a key role as host for multiple microorganism and virus without showing clinical manifestations of disease. After recognition of a potential threat, innate immunity triggers acute phase response, a systemic reaction that contributes to restrain microbial and viral growth. APR is characterized by fever, leukocytosis, and production of acute phase proteins, but also by behavioral changes, including somnolence, lethargy, and anorexia. Deploying immune responses, such as acute phase response, represents an energetic cost for vertebrates. In bats, it has been suggested that higher metabolic rates reached during flight might subsidize any inherent cost of raising metabolism to activate an immune response. Therefore, a central question is whether immune response represents a significant cost to bats and, if so, how much is the metabolic cost of these responses. Here, we assess the resting metabolic rate of Artibeus lituratus in response to challenge with LPS. In addition, we assessed parameters of acute phase response including fever, body mass loss, and leukocytosis in this specie. We found that challenge with LPS leads to an increase of 40% in resting metabolic rate of A. lituratus, concomitant with body mass loss and an increase in body temperature of 1.5 °C.


Artibeus lituratus Immune challenge Metabolic cost Bacterial lipopolysaccharide Acute phase response 



This research was supported by Vicerrectoría de Investigación Universidad del Valle CI 71027 and Posgrado en Ciencias Biología Universidad del Valle. We thank Dr. Luis Gerardo Herrera Montalvo for his critical reading of the manuscript and Alexander Torres MSc for his valuable advice on statistical analysis of data.

Compliance with ethical standards

This study was carried out according to recommendations and permits approved by the Permiso Marco de Recolección granted to the Universidad del Valle (Resolución 1070 de la Autoridad Nacional de Licencias Ambientales). Experimental procedures were reviewed and approved by the institutional ethics board for flora and fauna research of Universidad Del Valle.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13364_2018_375_MOESM2_ESM.docx (18 kb)
ESM 1 (DOCX 17 kb)
13364_2018_375_Fig5_ESM.gif (10 kb)
Supplementary fig. 1

The body mass of A. lituratus varies less than 10% during captivity. A. Percentage of body mass variation during captivity in individuals treated with LPS (n = 10). B. Percentage of body mass variation during captivity in individuals treated with PBS (n = 11) (GIF 9 kb)

13364_2018_375_MOESM1_ESM.tif (4.5 mb)
High resolution image (TIF 4604 kb)


  1. Akira S, Takeda K (2004) Toll-like receptor signalling. Nat Rev Immunol 4:499–511. CrossRefPubMedGoogle Scholar
  2. Baker ML, Schountz T, Wang LF (2013) Antiviral immune responses of bats: a review. Zoonoses Public Health 60:104–116. CrossRefPubMedGoogle Scholar
  3. Baumann H, Gauldie J (1994) The acute phase response. Immunol Today 15:74–80. CrossRefPubMedGoogle Scholar
  4. Berzunza-Cruz M, Rodríguez-Moreno Á, Gutiérrez-Granados G, González-Salazar C, Stephens CR, Hidalgo-Mihart M, Marina CF, Rebollar-Téllez EA, Bailón-Martínez D, Balcells CD, Ibarra-Cerdeña CN, Sánchez-Cordero V, Becker I (2015) Leishmania (L.) mexicana infected bats in Mexico: novel potential reservoirs. PLoS Negl Trop Dis 9:e0003438. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Beutler B (2000) Tlr4: central component of the sole mammalian LPS sensor. Curr Opin Immunol 12:20–26CrossRefPubMedGoogle Scholar
  6. Blander JM, Sander LE (2012) Beyond pattern recognition: five immune checkpoints for scaling the microbial threat. Nat Rev Immunol 12:215–225CrossRefPubMedGoogle Scholar
  7. Borek F (1987) The acute-phase response to injury and infection. The roles of interleukin 1 and other mediators: Gordon, AH and A. Koj (eds.), xxxii+ 340 pp., illus. Elsevier, Amsterdam, 1985. Dfl. 270, ISBN 0–444–80648-2Google Scholar
  8. Brogden KA, Cutlip RC, Lehmkuhl HD (1984) Response of sheep after localized deposition of lipopolysaccharide in the lung. Exp Lung Res 7:123–132CrossRefPubMedGoogle Scholar
  9. Brook CE, Dobson AP (2015) Bats as “ special ” reservoirs for emerging zoonotic pathogens. Trends Microbiol 23:172–180. CrossRefPubMedGoogle Scholar
  10. Bunnell JE, Hice CL, Watts DM, Montrueil V, Tesh RB, Vinetz JM (2000) Detection of pathogenic Leptospira spp. infections among mammals captured in the Peruvian Amazon basin region. Am J Trop Med Hyg 63:255–258CrossRefPubMedGoogle Scholar
  11. Burness G, Armstrong C, Fee T, Tilman-Schindel E (2010) Is there an energetic-based trade-off between thermoregulation and the acute phase response in zebra finches? J Exp Biol 213:1386–1394. CrossRefPubMedGoogle Scholar
  12. Cabrera-Martinez L, Herrera LG, Neto AC (2017) The energetic costs of mounting an immune response in Pallas’s long-tongued bat (Glossophaga soricina). PeerJ Prepr.
  13. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T (2006) Bats: important reservoir hosts of emerging viruses. Clin Microbiol Rev 19:531–545. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chua KB, Lek Koh C, Hooi PS, Wee KF, Khong JH, Chua BH, Chan YP, Lim ME, Lam SK (2002) Isolation of Nipah virus from Malaysian island flying-foxes. Microbes Infect 4:145–151. CrossRefPubMedGoogle Scholar
  15. Cray C, Zaias J, Altman NH (2009) Acute phase response in animals: a review. Comp Med 59:517–526PubMedPubMedCentralGoogle Scholar
  16. Dietrich M, Mühldorfer K, Tortosa P, Markotter W (2015) Leptospira and bats: story of an emerging friendship. PLoS Pathog 11:e1005176CrossRefPubMedPubMedCentralGoogle Scholar
  17. Evans SS, Repasky EA, Fisher DT (2015) Fever and the thermal regulation of immunity: the immune system feels the heat. Nat Rev Immunol 15:335–349CrossRefPubMedPubMedCentralGoogle Scholar
  18. Fox J, Weisberg S (2011) An {R} Companion to Applied Regression, Second. Sage, Thousand OaksGoogle Scholar
  19. Gabay C, Kushner I (1999) Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 340:448–454. CrossRefPubMedGoogle Scholar
  20. Gardner AL (2008) Mammals of South America, volume 1: marsupials, xenarthrans, shrews, and bats. University of Chicago PressGoogle Scholar
  21. Gomard Y, Dietrich M, Wieseke N, Ramasindrazana B, Lagadec E, Goodman SM, Dellagi K, Tortosa P (2016) Malagasy bats shelter a considerable genetic diversity of pathogenic Leptospira suggesting notable host-specificity patterns. FEMS Microbiol Ecol 92.
  22. Halpin K, Young PL, Field HE, Mackenzie JS (2000) Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus. J Gen Virol 81:1927–1932. CrossRefPubMedGoogle Scholar
  23. Hodo CL, Goodwin CC, Mayes BC, Mariscal JA, Waldrup KA, Hamer SA (2016) Trypanosome species, including Trypanosoma cruzi, in sylvatic and peridomestic bats of Texas, USA. Acta Trop 164:259–266. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefPubMedGoogle Scholar
  25. King MO, Swanson DL (2013) 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 216:2097–2102CrossRefPubMedGoogle Scholar
  26. Kovtun MF, Zhukova NF (1994) Feeding and digestion intensity in chiropterans of different trophic groups. Folia Zool 43:377–386Google Scholar
  27. Kuzmin I V, Schwarz TM, Ilinykh PA, Jordan I, Ksiazek TG, Sachidanandam R, Basler CF, Bukreyev A (2017) Innate immune response of bat and human cells to filoviruses: commonalities and distinctions. J Virol JVI--02471Google Scholar
  28. Lauvau G, Vijh S, Kong P, Horng T, Kerksiek K, Serbina N, Tuma RA, Pamer EG (2001) Priming of memory but not effector CD8 T cells by a killed bacterial vaccine. Science (80-) 294:1735–1739. CrossRefGoogle Scholar
  29. Leroy EM, Kumulungui B, Pourrut X, Rouquet P, Hassanin A, Yaba P, Délicat A, Paweska JT, Gonzalez J-P, Swanepoel R (2005) Fruit bats as reservoirs of Ebola virus. Nature 438:575–576. CrossRefPubMedGoogle Scholar
  30. Liegh Jr EG, Windsor MD (1982) Forest production and regulation of primary consumers on Barro Colorado island; inThe. Ecol a Trop For Seas Rhythm longterm Chang 111–122Google Scholar
  31. Lighton JRB (2008) Measuring metabolic rates: a manual for scientists. Oxford University PressGoogle Scholar
  32. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98. CrossRefGoogle Scholar
  33. MacDonald L, Begg D, Weisinger RS, Kent S (2012) Calorie restricted rats do not increase metabolic rate post-LPS, but do seek out warmer ambient temperatures to behaviourally induce a fever. Physiol Behav 107:762–772. CrossRefPubMedGoogle Scholar
  34. Marais M, Maloney SK, Gray DA (2011) The metabolic cost of fever in Pekin ducks. J Therm Biol 36:116–120. CrossRefGoogle Scholar
  35. Matthias MA, Díaz MM, Campos KJ, Calderon M, Willig MR, Pacheco V, Gotuzzo E, Gilman RH, Vinetz JM (2005) Diversity of bat-associated Leptospira in the Peruvian Amazon inferred by Bayesian phylogenetic analysis of 16S ribosomal DNA sequences. Am J Trop Med Hyg 73:964–974CrossRefPubMedPubMedCentralGoogle Scholar
  36. Middleton DJ, Morrissy CJ, Van Der HB, van der Heide BM, Russell GM, Braun MA, Westbury HA, Halpin K, Daniels PW (2007) Experimental Nipah virus infection in pteropid bats (Pteropus poliocephalus). J Comp Pathol 136:266–272. CrossRefPubMedGoogle Scholar
  37. Munster VJ, Adney DR, van Doremalen N, Brown VR, Miazgowicz KL, Milne-Price S, Bushmaker T, Rosenke R, Scott D, Hawkinson A, de Wit E, Schountz T, Bowen RA (2016) Replication and shedding of MERS-CoV in Jamaican fruit bats (Artibeus jamaicensis). Sci Rep 6:21878. CrossRefPubMedPubMedCentralGoogle Scholar
  38. O’Mara MT, Rikker S, Wikelski M, Ter Maat A, Pollock HS, Dechmann DKN (2017a) Heart rate reveals torpor at high body temperatures in lowland tropical free-tailed bats. R Soc Open Sci 4:171359. CrossRefPubMedPubMedCentralGoogle Scholar
  39. O’Mara MT, Wikelski M, Voigt CC, Ter Maat A, Pollock HS, Burness G, Desantis LM, Dechmann DKN (2017b) Cyclic bouts of extreme bradycardia counteract the high metabolism of frugivorous bats. elife.
  40. Otálora-Ardila A, Herrera ML, Flores-Martínez JJ, Welch KC (2016) 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 11:e0164938. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Paweska JT, Storm N, Grobbelaar AA, Markotter W, Kemp A, van Vuren P (2016) Experimental inoculation of Egyptian fruit bats (Rousettus aegyptiacus) with Ebola virus. Viruses 8:29CrossRefPubMedCentralGoogle Scholar
  42. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2017) {nlme}: Linear and nonlinear mixed effects modelsGoogle Scholar
  43. R Core Team (2017) R: A Language and Environment for Statistical ComputingGoogle Scholar
  44. Ramos Pereira MJ, Marques JT, Palmeirim JM (2010) Ecological responses of frugivorous bats to seasonal fluctuation in fruit availability in Amazonian forests. Biotropica 42:680–687. CrossRefGoogle Scholar
  45. Schneeberger K, Czirják GÁ, Voigt CC (2013) Inflammatory challenge increases measures of oxidative stress in a free-ranging, long-lived mammal. J Exp Biol 216:4514–4519. CrossRefPubMedGoogle Scholar
  46. Schneeberger K, Voigt CC (2013) Measures of the constitutive immune system are linked to diet and roosting habits of neotropical bats measures of the constitutive immune system are linked to diet and roosting habits of neotropical bats.
  47. Sikes RS, Gannon WL (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92:235–253. CrossRefGoogle Scholar
  48. Smith DJW, Mackerras IM (1964) The epidemiology of leptospirosis in North Queensland: I. General survey of animal hosts. J Hyg (Lond) 62:451–484. CrossRefGoogle Scholar
  49. Speakman JR, Król E (2010) Maximal heat dissipation capacity and hyperthermia risk: Neglected key factors in the ecology of endothermsGoogle Scholar
  50. Stockmaier S, Dechmann DKN, Page RA, O’Mara MT (2015) No fever and leucocytosis in response to a lipopolysaccharide challenge in an insectivorous bat. Biol Lett 11:4–7. CrossRefGoogle Scholar
  51. Tulsiani SM, Cobbold RN, Graham GC, Dohnt MF, Burns M, Leung LK, Field HE, Smythe LD, Craig SB (2011) The role of fruit bats in the transmission of pathogenic leptospires in Australia. Ann Trop Med Parasitol 105:71–84. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Vance RE, Isberg RR, Portnoy DA (2009) Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6:10–21CrossRefPubMedPubMedCentralGoogle Scholar
  53. Viney ME, Riley EM (2014) From immunology to eco-immunology: more than a new name. In: Eco-immunology. Springer, pp 1–19Google Scholar
  54. Von Koenig CHW, Finger H, Hof H (1982) Failure of killed listeria monocytogenes vaccine to produce protective immunity. Nature 297:233–234. CrossRefGoogle Scholar
  55. Weise P, Czirják GA, Lindecke O, Bumrungsri S, Voigt CC (2017) Simulated bacterial infection disrupts the circadian fluctuation of immune cells in wrinkle-lipped bats (Chaerephon plicatus). PeerJ 5:e3570CrossRefPubMedPubMedCentralGoogle Scholar
  56. Williamson MM, Hooper PT, Selleck PW, Gleeson LJ, Daniels PW, Westbury HA, Murray PK (1998) Transmission studies of Hendra virus (equine morbillivirus) in fruit bats, horses and cats. Aust Vet J 76:813–818. CrossRefPubMedGoogle Scholar
  57. Wilson DE and DMR (2005) Mammal species of the world : a taxonomic and geographic reference. Balt. Johns Hopkins Univ. Press 312_529Google Scholar
  58. Zortéa M, Mendes SL (1993) Folivory in the big fruit-eating bat, artiheus lituratus (chiroptera: Phyllostomidae) in eastern Brazil. J Trop Ecol 9:117–120. CrossRefGoogle Scholar

Copyright information

© Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2018

Authors and Affiliations

  • Adriana L. Guerrero-Chacón
    • 1
  • David Rivera-Ruíz
    • 1
  • Vladimir Rojas-Díaz
    • 2
  • Camila Triana-Llanos
    • 1
  • Andrea Niño-Castro
    • 1
  1. 1.Laboratorio de Fisiología Animal, Departamento de BiologíaUniversidad del ValleCaliColombia
  2. 2.Wildlife Conservation SocietyCaliColombia

Personalised recommendations