Journal of Comparative Physiology B

, Volume 187, Issue 1, pp 213–226 | Cite as

Does diet influence salivary enzyme activities in elephant species?

  • Carolin Boehlke
  • Sandra Pötschke
  • Verena Behringer
  • Christian Hannig
  • Oliver Zierau
Original Paper

Abstract

Asian elephants (Elephas maximus) and African elephants (Loxodonta africana) are herbivore generalists; however, Asian elephants might ingest a higher proportion of grasses than Africans. Although some studies have investigated nutrition-specific morphological adaptations of the two species, broader studies on salivary enzymes in both elephant species are lacking. This study focuses on the comparison of salivary enzymes activity profiles in the two elephant species; these enzymes are relevant for protective and digestive functions in humans. We aimed to determine whether salivary amylase (sAA), lysozyme (sLYS), and peroxidase (sPOD) activities have changed in a species-specific pattern during evolutionary separation of the elephant genera. Saliva samples of 14 Asian and eight African elephants were collected in three German zoos. Results show that sAA and sLYS are salivary components of both elephant species in an active conformation. In contrast, little to no sPOD activity was determined in any elephant sample. Furthermore, sAA activity was significantly higher in Asian compared with African elephants. sLYS and sPOD showed no species-specific differences. The time of food provision until sample collection affected only sAA activity. In summary, the results suggest several possible factors modulating the activity of the mammal-typical enzymes, such as sAA, sLYS, and sPOD, e.g., nutrition and sampling procedure, which have to be considered when analyzing differences in saliva composition of animal species.

Keywords

Elephant Salivary enzyme activity Amylase Nutrition Evolution 

References

  1. Abell AD, Ratcliffe MJ, Gerrard J (1998) Ascorbic acid-based inhibitors of α-amylases. Bioorg Med Chem Lett 8:1703–1706. doi:10.1016/S0960-894X(98)00298-4 CrossRefPubMedGoogle Scholar
  2. Ang C-S, Binos S, Knight MI et al (2011) Global survey of the bovine salivary proteome: integrating multidimensional prefractionation, targeted, and glycocapture strategies. J Proteome Res 10:5059–5069. doi:10.1021/pr200516d CrossRefPubMedGoogle Scholar
  3. Banerjee RK, Datta AG (1986) Salivary peroxidases. Mol Cell Biochem 70:21–29CrossRefPubMedGoogle Scholar
  4. Barabash RD, Gukevich EK, Berezovskaia ZV et al (1979) Role of peroxidase in the pathogenesis of parodontosis. Vopr meditsinskoi Khimii 25:333–342Google Scholar
  5. Battino M, Ferreiro MS, Gallardo I et al (2002) The antioxidant capacity of saliva. J Clin Periodontol 29:189–194CrossRefPubMedGoogle Scholar
  6. Becerra L, Soares RV, Bruno LS et al (2003) Patterns of secretion of mucins and non-mucin glycoproteins in human submandibular/sublingual secretion. Arch Oral Biol 48:147–154. doi:10.1016/S0003-9969(02)00171-1 CrossRefPubMedGoogle Scholar
  7. Bird JL, Baum BJ, Makinen KK et al (1977) Xylitol associated changes in amylase and protein content of monkey parotid saliva. J Nutr 107:1763–1767PubMedGoogle Scholar
  8. Björck L, Rosén C, Marshall V, Reiter B (1975) Antibacterial activity of the lactoperoxidase system in milk against pseudomonads and other gram-negative bacteria. Appl Microbiol 30:199–204PubMedPubMedCentralGoogle Scholar
  9. Black MJ, Brandt RB (1974) Spectrofluorometric analysis of hydrogen peroxide. Anal Biochem 58:246–254CrossRefPubMedGoogle Scholar
  10. Blanc JJ, Barnes RFW, Craig CG, et al (2007) African elephant status report 2007: an update from the African elephant database. no. 33. Occas. Pap. IUCN Species Surviv. Comm. IUCNSSC Afr. Elephant Spec. GroupGoogle Scholar
  11. Boehlke C, Zierau O, Hannig C (2015) Salivary amylase—The enzyme of unspecialized euryphagous animals. Arch Oral Biol 60:1162–1176. doi:10.1016/j.archoralbio.2015.05.008 CrossRefPubMedGoogle Scholar
  12. Butterworth PJ, Warren FJ, Ellis PR (2011) Human α-amylase and starch digestion: an interesting marriage. Starch Stärke 63:395–405. doi:10.1002/star.201000150 CrossRefGoogle Scholar
  13. Carpenter GH (2013) The secretion, components, and properties of saliva. Annu Rev Food Sci Technol 4:267–276. doi:10.1146/annurev-food-030212-182700 CrossRefPubMedGoogle Scholar
  14. Cerling TE, Harris JM, Leakey MG (1999) Browsing and grazing in elephants: the isotope record of modern and fossil proboscideans. Oecologia 120:364–374CrossRefGoogle Scholar
  15. Clauss M, Frey R, Kiefer B et al (2003) The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters. Oecologia 136:14–27. doi:10.1007/s00442-003-1254-z CrossRefPubMedGoogle Scholar
  16. Clauss M, Gehrke J, Hatt J-M et al (2005) Tannin-binding salivary proteins in three captive rhinoceros species. Comp Biochem Physiol A: Mol Integr Physiol 140:67–72. doi:10.1016/j.cbpb.2004.11.005 CrossRefGoogle Scholar
  17. Clauss M, Steinmetz H, Eulenberger U et al (2007) Observations on the length of the intestinal tract of African Loxodonta africana (Blumenbach 1797) and Asian elephants Elephas maximus (Linné 1735). Eur J Wildl Res 53:68–72. doi:10.1007/s10344-006-0064-0 CrossRefGoogle Scholar
  18. Clements S, Mehansho H, Carlson DM (1985) Novel multigene families encoding highly repetitive peptide sequences. Sequence analyses of rat and mouse proline-rich protein cDNAs. J Biol Chem 260:13471–13477PubMedGoogle Scholar
  19. Codron J, Lee-Thorp JA, Sponheimer M et al (2006) Elephant (Loxodonta africana) diets in Kruger National Park, South Africa: spatial and landscape differences. J Mammal 87:27–34. doi:10.1644/05-MAMM-A-017R1.1 CrossRefGoogle Scholar
  20. Codron J, Codron D, Sponheimer M et al (2012) Stable isotope series from elephant ivory reveal lifetime histories of a true dietary generalist. Proc R Soc B Biol Sci 279:2433–2441. doi:10.1098/rspb.2011.2472 CrossRefGoogle Scholar
  21. da Costa G, Lamy E, Capela E, Silva F et al (2008) Salivary amylase induction by tannin-enriched diets as a possible countermeasure against tannins. J Chem Ecol 34:376–387. doi:10.1007/s10886-007-9413-z CrossRefPubMedGoogle Scholar
  22. Dastjerdi A, Robert C, Watson M (2014) Low coverage sequencing of two Asian elephant (Elephas maximus) genomes. GigaScience 3:12CrossRefPubMedPubMedCentralGoogle Scholar
  23. De Boer WF, Ntumi CP, Correia AU, Mafuca JM (2000) Diet and distribution of elephant in the Maputo Elephant Reserve, Mozambique. Afr J Ecol 38:188–201CrossRefGoogle Scholar
  24. Dhindsa DS, Sedgwick CJ, Metcalfe J (1972) Comparative studies of the respiratory functions of mammalian blood. VIII. Asian elephant (Elephas maximus) and African elephant (Loxodonta africana africana). Respir Physiol 14:332–342. doi:10.1016/0034-5687(72)90038-2 CrossRefPubMedGoogle Scholar
  25. Falchi M, El-Sayed Moustafa JS, Takousis P et al (2014) Low copy number of the salivary amylase gene predisposes to obesity. Nat Genet 46:492–497. doi:10.1038/ng.2939 CrossRefPubMedGoogle Scholar
  26. Fickel J, Göritz F, Joest BA et al (1998) Analysis of parotid and mixed saliva in roe deer (Capreolus capreolus l.). J Comp Physiol B 168:257–264CrossRefPubMedGoogle Scholar
  27. Gheerbrant E (2009) Paleocene emergence of elephant relatives and the rapid radiation of African ungulates. Proc Natl Acad Sci 106:10717–10721CrossRefPubMedPubMedCentralGoogle Scholar
  28. Green JL (1995) The use of lysozyme in winemaking: the interaction of lysozyme with wine and efficacy in preventing malolactic fermentation in Oregon Pinot noir and Chardonnay. Master Thesis. Oregon State UniversityGoogle Scholar
  29. Guy PR (1976) The feeding behaviour of elephant (Loxodonta africana) in the Sengwa area, Rhodesia. South Afr J Wildl Res 6:55–63Google Scholar
  30. Hannig C, Attin T, Hannig M et al (2004) Immobilisation and activity of human α-amylase in the acquired enamel pellicle. Arch Oral Biol 49:469–475. doi:10.1016/j.archoralbio.2004.01.005 CrossRefPubMedGoogle Scholar
  31. Hannig C, Hannig M, Attin T (2005) Enzymes in the acquired enamel pellicle. Eur J Oral Sci 113:2–13. doi:10.1111/j.1600-0722.2004.00180.x CrossRefPubMedGoogle Scholar
  32. Hannig C, Spitzmüller B, Knausenberger S et al (2008) Detection and activity of peroxidase in the in situ formed enamel pellicle. Arch Oral Biol 53:849–858. doi:10.1016/j.archoralbio.2008.03.003 CrossRefPubMedGoogle Scholar
  33. Hummel J, Südekum K-H, Streich WJ, Clauss M (2006) Forage fermentation patterns and their implications for herbivore ingesta retention times. Funct Ecol 20:989–1002. doi:10.1111/j.1365-2435.2006.01206.x CrossRefGoogle Scholar
  34. Humphrey SP, Williamson RT (2001) A review of saliva: normal composition, flow, and function. J Prosthet Dent 85:162–169. doi:10.1067/mpr.2001.113778 CrossRefPubMedGoogle Scholar
  35. Ihalin R, Loimaranta V, Tenovuo J (2006) Origin, structure, and biological activities of peroxidases in human saliva. Arch Biochem Biophys 445:261–268. doi:10.1016/j.abb.2005.07.004 CrossRefPubMedGoogle Scholar
  36. Illera J-C, Silván G, Cáceres S et al (2014) Assessment of ovarian cycles in the African elephant (loxodonta africana) by measurement of salivary progesterone metabolites: elephant cycle salivary progestins. Zoo Biol 33:245–249. doi:10.1002/zoo.21124 CrossRefPubMedGoogle Scholar
  37. IUCN (2008) Elephas maximus: Choudhury A, Lahiri Choudhury DK, Desai A, Duckworth JW, Easa PS, Johnsingh AJT, Fernando P, Hedges S, Gunawardena M, Kurt F, Karanth U, Lister A, Menon V, Riddle H, Rübel A; Wikramanayake E (IUCN SSC Asian Elephant Specialist Group): The IUCN Red List of Threatened Species 2008: e.T7140A12828813Google Scholar
  38. Joshi R, Singh R (2008) Feeding behaviour of wild Asian elephants (Elephas maximus) in the Rajaji National Park. J Am Sci 4:34–48Google Scholar
  39. Kabigumila J (1993) Feeding habits of elephants in Ngorongoro Crater, Tanzania. Afr J Ecol 31:156–164. doi:10.1111/j.1365-2028.1993.tb00528.x CrossRefGoogle Scholar
  40. Kaufman E, Lamster IB (2000) Analysis of saliva for periodontal diagnosis. J Clin Periodontol 27:453–465CrossRefPubMedGoogle Scholar
  41. Koch PL, Heisinger J, Moss C et al (1995) Isotopic tracking of change in diet and habitat use in african elephants. Science 267:1340–1343. doi:10.1126/science.267.5202.1340 CrossRefPubMedGoogle Scholar
  42. Koh D, Ng V, Naing L (2014) Alpha amylase as a salivary biomarker of acute stress of venepuncture from periodic medical examinations. Front Public Health. doi:10.3389/fpubh.2014.00121 Google Scholar
  43. Laible NJ, Germaine GR (1985) Bactericidal activity of human lysozyme, muramidase-inactive lysozyme, and cationic polypeptides against Streptococcus sanguis and Streptococcus faecalis: inhibition by chitin oligosaccharides. Infect Immun 48:720–728PubMedPubMedCentralGoogle Scholar
  44. Laursen L, Bekoff M (1978) Loxodonta africana. Mamm. Species 92:1–8CrossRefGoogle Scholar
  45. Lima DP, Diniz DG, Moimaz SAS et al (2010) Saliva: reflection of the body. Int J Infect Dis 14:e184–e188. doi:10.1016/j.ijid.2009.04.022 CrossRefPubMedGoogle Scholar
  46. Luca F, Perry GH, Di Rienzo A (2010) Evolutionary adaptations to dietary changes. Annu Rev Nutr 30:291–314. doi:10.1146/annurev-nutr-080508-141048 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Mackie DA, Pangborn RM (1990) Mastication and its influence on human salivary flow and alpha-amylase secretion. Physiol Behav 47:593–595. doi:10.1016/0031-9384(90)90131-M CrossRefPubMedGoogle Scholar
  48. Mäkinen KK, Bowen WH, Dalgard D, Fitzgerald G (1978) Effect of peroral administration of xylitol on exocrine secretions of monkeys. J Nutr 108:779–789PubMedGoogle Scholar
  49. Mandel AL, des Gachons CP, Plank KL et al (2010) Individual differences in amy1 gene copy number, salivary α-amylase levels, and the perception of oral starch. PLoS One 5:e13352. doi:10.1371/journal.pone.0013352 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Marcilla AM, Urios V, Limiñana R (2012) Seasonal rhythms of salivary cortisol secretion in captive Asian elephants (Elephas maximus). Gen Comp Endocrinol 176:259–264. doi:10.1016/j.ygcen.2012.02.001 CrossRefGoogle Scholar
  51. Mason G, Rushen J (eds) (2006) Stereotypic animal behaviour: fundamentals and applications to welfare, 2nd edn. CABI Pub, Wallingford, UK, CambridgeGoogle Scholar
  52. Mau M, Südekum K-H, Johann A et al (2009) Saliva of the graminivorous Theropithecus gelada lacks proline-rich proteins and tannin-binding capacity. Am J Primatol 71:663–669. doi:10.1002/ajp.20701 CrossRefPubMedGoogle Scholar
  53. Mau M, Südekum K-H, Johann A et al (2010) Indication of higher salivary α-amylase expression in hamadryas baboons and geladas compared to chimpanzees and humans: salivary amylase in primates and humans. J Med Primatol 39:187–190. doi:10.1111/j.1600-0684.2010.00407.x CrossRefPubMedGoogle Scholar
  54. Mau M, Kaiser TM, Südekum K-H (2013) Pilot study on binding of bovine salivary proteins to grit silicates and plant phytoliths. Zool Res 34:87–92Google Scholar
  55. Mehansho H, Clements S, Sheares BT et al (1985) Induction of proline-rich glycoprotein synthesis in mouse salivary glands by isoproterenol and by tannins. J Biol Chem 260:4418–4423PubMedGoogle Scholar
  56. Mohapatra KK, Patra AK, Paramanik DS (2013) Food and feeding behaviour of Asiatic elephant (Elephas maximus Linn.) in Kuldiha Wild Life Sanctuary, Odisha, India. J Environ Biol Acad Environ Biol India 34:87–92Google Scholar
  57. Morishita Y, Iinuma Y, Nakashima N et al (2000) Total and pancreatic amylase measured with 2-chloro-4-nitrophenyl-4-O-β-d-galactopyranosylmaltoside. Clin Chem 46:928–933PubMedGoogle Scholar
  58. Nater UM, Rohleder N (2009) Salivary alpha-amylase as a non-invasive biomarker for the sympathetic nervous system: current state of research. Psychoneuroendocrinology 34:486–496. doi:10.1016/j.psyneuen.2009.01.014 CrossRefPubMedGoogle Scholar
  59. Nater UM, Rohleder N, Gaab J et al (2005) Human salivary alpha-amylase reactivity in a psychosocial stress paradigm. Int J Psychophysiol 55:333–342. doi:10.1016/j.ijpsycho.2004.09.009 CrossRefPubMedGoogle Scholar
  60. Neyraud E, Sayd T, Morzel M, Dransfield E (2006) Proteomic analysis of human whole and parotid salivas following stimulation by different tastes. J Proteome Res 5:2474–2480. doi:10.1021/pr060189z CrossRefPubMedGoogle Scholar
  61. Noble RE (2000) Salivary alpha-amylase and lysozyme levels: a non-invasive technique for measuring parotid vs submandibular/sublingual gland activity. J Oral Sci 42:83–86CrossRefPubMedGoogle Scholar
  62. Oberg SG, Izutsu KT, Truelove EL (1982) Human parotid saliva protein composition: dependence on physiological factors. Am J Physiol-Gastrointest Liver Physiol 242:G231–G236Google Scholar
  63. Perry GH, Dominy NJ, Claw KG et al (2007) Diet and the evolution of human amylase gene copy number variation. Nat Genet 39:1256–1260. doi:10.1038/ng2123 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Polyzois S, Baum BJ, Bowen WH, Longton RW (1976) Differences in the ph activity profile of human and monkey salivary lysozyme. J Dent Res 55:1137. doi:10.1177/00220345760550063101 CrossRefPubMedGoogle Scholar
  65. Proctor GB, Chan K-M (1994) A fluorometric assay of peroxidase activity utilizing 2′,7′-dichlorofluorescein with thiocyanate: application to the study of salivary secretion. J Biochem Biophys Methods 28:69–76CrossRefPubMedGoogle Scholar
  66. Pruitt KM, Adamson M (1977) Enzyme activity of salivary lactoperoxidase adsorbed to human enamel. Infect Immun 17:112–116PubMedPubMedCentralGoogle Scholar
  67. Raubenheimer EJ, Dauth J, Dreyer MJ, de Vos V (1988) Parotid salivary gland of the African elephant (Loxodonta africana): structure and composition of saliva. J S Afr Vet Assoc 59:184–187PubMedGoogle Scholar
  68. Robbins CT (1983) Wildlife feeding and nutrition. Academic Press, New York, p 235Google Scholar
  69. Rodiek A (2010) Optimizing different hay types for horses: what have we learned? Proceedings, 2010 California Alfalfa & Forage Symposium and Corn/Cereal Silage Mini-Symposium. Visalia, CAGoogle Scholar
  70. Rohland N, Malaspinas A-S, Pollack JL et al (2007) Proboscidean mitogenomics: chronology and mode of elephant evolution using mastodon as outgroup. PLoS Biol 5:e207. doi:10.1371/journal.pbio.0050207 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Rohleder N, Nater UM (2009) Determinants of salivary α-amylase in humans and methodological considerations. Psychoneuroendocrinology 34:469–485. doi:10.1016/j.psyneuen.2008.12.004 CrossRefPubMedGoogle Scholar
  72. Sanson G (2006) The biomechanics of browsing and grazing. Am J Bot 93:1531–1545CrossRefPubMedGoogle Scholar
  73. Schlueter N, Ganss C, Pötschke S et al (2012) Enzyme activities in the oral fluids of patients suffering from bulimia: a controlled clinical trial. Caries Res 46:130–139. doi:10.1159/000337105 CrossRefPubMedGoogle Scholar
  74. Shackleford JM, Klapper CE (1962) Structure and carbohydrate histochemistry of mammalian salivary glands. Am J Anat 111:25–47CrossRefPubMedGoogle Scholar
  75. Shimada T (2006) Salivary proteins as a defense against dietary tannins. J Chem Ecol 32:1149–1163. doi:10.1007/s10886-006-9077-0 CrossRefPubMedGoogle Scholar
  76. Shipley LA (1999) Grazers and browsers: how digestive morphology affects diet selection. In: Launchbaugh KL, Sanders KD, Mosley JC (eds) Grazing behavior of livestock and wildlife. Presented in: “Grazing Behavior of Livestock and Wildlife.” 1999. Idaho Forest, Wildlife & Range Exp. Sta. Bull. 70, Univ. of Idaho, Moscow, ID, pp 20–27Google Scholar
  77. Shoshani J, Eisenberg JF (1982) Elephas maximus. Mamm. Species 182:1–8CrossRefGoogle Scholar
  78. Sreebny LM (2000) Saliva in health and disease: an appraisal and update. Int Dent J 50:140–161CrossRefPubMedGoogle Scholar
  79. Steele WF, Morrison M (1969) Antistreptococcal activity of lactoperoxidase. J Bacteriol 97:635–639PubMedPubMedCentralGoogle Scholar
  80. Sukumar R (1989) The Asian elephant: ecology and management. Cambridge studies in applied ecology and resource management. Cambridge University Press, CambridgeGoogle Scholar
  81. Todd NE (2010) Qualitative comparison of the cranio-dental osteology of the extant elephants, Elephas maximus (Asian elephant) and Loxodonta africana (African elephant). Anat Rec Adv Integr Anat Evol Biol 293:62–73. doi:10.1002/ar.21011 CrossRefGoogle Scholar
  82. Touger-Decker R, Van Loveren C (2003) Sugars and dental caries. Am J Clin Nutr 78:881S–892SPubMedGoogle Scholar
  83. Ullrey DE, Crissey SD, Hintz HF (1997) Elephants: nutrition and dietary husbandry. Nutrition Advisory Group. Michigan State University. http://wildpro.twycrosszoo.org/000ADOBES/Elephants/D297nutrdietEle_NAG.pdf. Accessed 23 July 2015
  84. van Sonsbeek GR, van der Kolk JH, van Leeuwen JPTM et al (2013) Effect of calcium and cholecalciferol supplementation on several parameters of calcium status in plasma and urine of captive Asian (Elephas maximus) and African elephants (Loxodonta africana). J Zoo Wildl Med Off Publ Am Assoc Zoo Vet 44:529–540. doi:10.1638/2010-0123R4.1 Google Scholar
  85. Veerman ECI, Keybus PAM, Vissink A, Amerongen AVN (1996) Human glandular salivas: their separate collection and analysis. Eur J Oral Sci 104:346–352. doi:10.1111/j.1600-0722.1996.tb00090.x CrossRefPubMedGoogle Scholar
  86. Vray B, Hoebeke J, Saint-Guillain M et al (1980) A new quantitative fluorimetric assay for phagocytosis of bacteria. Scand J Immunol 11:147–153. doi:10.1111/j.1365-3083.1980.tb00220.x CrossRefPubMedGoogle Scholar
  87. Wang Y-B, Germaine GR (1993) Effects of pH, potassium, magnesium, and bacterial growth phase on lysozyme inhibition of glucose fermentation by Streptococcus mutans. J Dent Res 72:907–911CrossRefPubMedGoogle Scholar
  88. Watt RG (2005) Strategies and approaches in oral disease prevention and health promotion. Bull World Health Organ 83:711–718PubMedPubMedCentralGoogle Scholar
  89. Wheeler TT, Haigh BJ, Broadhurst MK et al (2011) The BPI-like/PLUNC family proteins in cattle. Biochem Soc Trans 39:1006–1011. doi:10.1042/BST0391006 CrossRefPubMedGoogle Scholar
  90. Wing LD, Buss IO (1970) Elephants and forests. Wildl Monogr 19:3–92Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Carolin Boehlke
    • 1
    • 2
  • Sandra Pötschke
    • 1
  • Verena Behringer
    • 3
  • Christian Hannig
    • 1
  • Oliver Zierau
    • 2
  1. 1.Policlinic of Operative and Pediatric Dentistry, Faculty of Medicine ‘Carl Gustav Carus’TU DresdenDresdenGermany
  2. 2.Institute of Zoology, Molecular Cell Physiology and EndocrinologyTU DresdenDresdenGermany
  3. 3.Department of PrimatologyMax Planck Institute for Evolutionary AnthropologyLeipzigGermany

Personalised recommendations