Skip to main content
SpringerLink
Log in

Membrane-bound intestinal enzymes of passerine birds: dietary and phylogenetic correlates

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Bird species exhibit great diversity in digestive tract morphology and enzymatic activity that is partly correlated with the chemical composition of their natural diets. However, no studies have assessed whether the activities of digestive enzymes of the enterocytes correlate with dietary chemical composition data analyzed as a continuous variable at an evolutionary scale. We used a phylogenetically explicit approach to examine the effect of diet on the hydrolytic activity of three digestive enzymes (maltase, sucrase, and aminopeptidase-N) in 16 species of songbirds (Order Passeriformes) from Central Chile. The total activities (μmol/min) of these enzymes were positively associated with body mass using both conventional least squares regressions and phylogenetically independent contrasts. After removing mass effects, we found a significant negative correlation between the ratio of aminopeptidase-N and maltase to the proportion of seeds found in the gizzard, but this relationship was no longer significant after controlling for phylogeny. When we analyzed the specific nutritional content of the diet, we found that the percentage of nitrogen in diet was negatively correlated with residual maltase activity and positively correlated with the ratio aminopeptidase-N/maltase. Given the large interspecific differences in biochemical capacity, we conclude that these differences reflect genetically determined evolutionary changes associated with the nutrient contents of each species’ natural diet.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

APN:

Aminopeptidase-N

LSI :

Length of the small intestine

m b :

Body mass (g)

M SI :

Mass of the small intestine

PIC:

Phylogenetical independent contrast

CLSR:

Conventional least square regression

References

  • Ackerly D (2009) Conservatism and diversification of plant functional traits: evolutionary rates versus phylogenetic signal. Proc Natl Acad Sci USA 17:19699–19706

    Article  Google Scholar 

  • Afik D, Caviedes-Vidal E, Martínez del Rio C, Karasov WH (1995) Dietary modulation of intestinal hydrolytic enzymes in Yellow-rumped warblers. Am J Physiol 269:R413–R420

    PubMed  CAS  Google Scholar 

  • American Ornithologist Union (1988) Guidelines for use of wild birds in research. Auk 105:1a–41a

    Google Scholar 

  • Barker FK, Cibois A, Schikler P, Feinstein J, Cracraft J (2004) Phylogeny and diversification of the largest avian radiation. Proc Natl Acad Sci USA 101:11040–11045

    Article  PubMed  CAS  Google Scholar 

  • Biviano AB, Martínez del Rio C, Phillips DL (1993) Ontogenesis of intestine morphology and intestinal disaccharidases in chickens (Gallus gallus) fed contrasting purified diets. J Comp Physiol B 163:508–518

    PubMed  CAS  Google Scholar 

  • Blomberg SP, Garland T Jr, Ives A (2003) Testing for phylogenetic signal in comparative data: behavioural traits are labile. Evolution 57:717–745

    PubMed  Google Scholar 

  • Bozinovic F, Muñoz-Pedreros A (1995) Nutritional ecology and digestive responses of an omnivorous-insectivorous rodent (Abrothrix longipilis) feeding on fungus. Physiol Zool 68:474–489

    Google Scholar 

  • Brzek P, Kohl K, Caviedes-Vidal E, Karasov WH (2009) Developmental adjustments of house sparrow (Passer domesticus) nestlings to diet composition. J Exp Biol 212:1284–1293

    Article  PubMed  CAS  Google Scholar 

  • Brzek P, Lessner KM, Caviedes-Vidal E, Karasov WH (2010) Low plasticity in digestive physiology constrains feeding ecology in diet specialist, zebra finch (Taeniopygia guttata). J Exp Biol 213:798–807

    Article  PubMed  CAS  Google Scholar 

  • Buddington RK, Chen JW, Diamond J (1987) Genetic and phenotypic adaptation of intestinal nutrient transport to diet in fish. J Physiol 393:261–281

    PubMed  CAS  Google Scholar 

  • Caviedes-Vidal E, Karasov WH (2001) Developmental changes in digestive physiology of nestling house sparrows, Passer domesticus. Physiol Biochem Zool 74:769–782

    Article  PubMed  CAS  Google Scholar 

  • Caviedes-Vidal E, Afik D, Martínez del Rio C, Karasov WH (1994) Omnivory and dietary plasticity are not necessarily correlated: dietary modulation of intestinal enzymes in four bird species. Physiologist 37:A81

    Google Scholar 

  • Caviedes-Vidal E, Afik D, Martínez del Rio C, Karasov WH (2000) Dietary modulation of intestinal enzymes of the house sparrow (Passer domesticus): testing an adaptative hypothesis. Comp Biochem Physiol A 125:11–24

    CAS  Google Scholar 

  • Cheverud JM, Dow MM, Leutenneger W (1985) The quantitative assessment of phylogenetic constraints in comparative analysis sexual dimorphism in body weight among primates. Evolution 6:1335–1351

    Article  Google Scholar 

  • Cruz-Neto AP, Bozinovic F (2004) The relationships between diet quality and basal metabolic rate in endotherms: insights from intraspecific analysis. Physiol Biochem Zool 77:877–889

    Article  PubMed  Google Scholar 

  • Cruz-Neto AP, Garland T Jr, Abe AS (2001) Diet, phylogeny and basal metabolic rate in phyllostomid bats. Zoology 104:49–58

    Article  PubMed  CAS  Google Scholar 

  • Dahlqvist A (1964) Assay of intestinal disaccharidases. Scand J Clin Lab Invest 44:69–172

    Google Scholar 

  • Diamond JM, Hammond KA (1992) The matches, achieved by natural selection, between biological capacities and their natural loads. Experientia 48:551–557

    Article  PubMed  CAS  Google Scholar 

  • Fain MG, Houde P (2004) Parallel radiations in the primary clades of birds. Evolution 58:2558–2573

    PubMed  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Freckleton RP, Harvey HP, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    Article  PubMed  CAS  Google Scholar 

  • Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Google Scholar 

  • Gartrell BD (2000) The nutritional, morphologic, and physiologic bases of nectarivory in Australian birds. J Av Med Surg 14:85–94

    Article  Google Scholar 

  • Gonzalez J, Wink M (2008) Phylogenetic position of the monotypic DesMurs’Wiretail (Sylviorthorhynchus desmursii, Aves: Furnariidae) based on mitochondrial and nuclear DNA. J Ornithol 149:393–398

    Article  Google Scholar 

  • Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2009) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768

    Article  Google Scholar 

  • Hume ID (1998) Optimization in design of the digestive system. In: Weibel ER, Taylor CR, Bolis L (eds) Principles of animal design. Cambridge University Press, Cambridge, pp 212–219

    Google Scholar 

  • Jaksic F (2001) Spatiotemporal variation patterns of plants and animals in San Carlos de Apoquindo, central Chile. Rev Chil Hist Nat 74:477–502

    Article  Google Scholar 

  • Karasov WH, Diamond JM (1988) Interplay between physiology and ecology in digestion. Bioscience 38:602–611

    Article  CAS  Google Scholar 

  • Karasov WH, Levey DJ (1990) Digestive system trade-offs and adaptations of frugivorous passerine birds. Physiol Zool 63:1248–1270

    Google Scholar 

  • Karasov WH, Martínez del Rio C (2007) Physiological ecology: How animals process energy, nutrients and toxins. Princeton University Press, Princeton

    Google Scholar 

  • Karasov WH, Afik D, Darken BW (1996) Do northern bobwhite quail modulate intestinal nutrient absorption in response to dietary change? A test of an adaptational hypothesis. Comp Biochem Physiol A 113:233–238

    Article  Google Scholar 

  • Klasing KC (1998) Comparative avian nutrition. CAB International

  • Lanyon SM, Omland KE (1999) A molecular phylogeny of the blackbirds (Icteridae): five lineages revealed by cytochrome-b sequence data. Auk 116:629–639

    Google Scholar 

  • Levey DJ, Place AR, Rey PJ, Martinez del Rio C (1999) An experimental test of dietary enzyme modulation in pine warblers Dendroica pinus. Physiol Biochem Zool 72:576–587

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Calleja MV (1995) Dieta de Zonotrichia capensis (Emberizidae) and Diuca diuca (Fringillidae): efecto de la variación estacional de los recursos tróficos y la riqueza de aves granívoras de Chile central. Rev Chil Hist Nat 68:321–331

    Google Scholar 

  • Lopez-Calleja MV, Bozinovic F, Martínez del Rio C (1997) Effects of sugar concentration on hummingbird feeding and energy use. Comp Biochem Physiol A 118:1291–1299

    Article  Google Scholar 

  • Martínez del Rio C (1990) Dietary and phylogenetic correlates of intestinal sucrose and maltase activity in birds. Physiol Zool 63:987–1011

    Google Scholar 

  • Martínez del Rio C, Karasov WH (1990) Digestion strategies in nectar-and-fruit eating and the sugar composition of plant rewards. Am Nat 136:618–637

    Article  Google Scholar 

  • Martínez del Rio C, Stevens BR (1989) Physiological constraint on feeding behavior: intestinal membrane disaccharidases of the starlings. Science 43:794–796

    Article  Google Scholar 

  • Martínez del Rio C, Baker HG, Baker I (1992) Ecological and evolutionary implication of digestive processes: bird preferences and sugar constituents of floral nectar and fruit pulp. Experentia 48:540–544

    Google Scholar 

  • Martínez del Rio C, Brugger K, Witmer M, Riors J, Vergara E (1995) An experimental and comparative study of dietary modulation of intestinal enzymes in European starlings (Sturnus vulgaris). Physiol Zool 68:490–511

    Google Scholar 

  • McNab BK (1992) The comparative energetics of rigid endothermy: the Arvicolidae. J Zool 227:586–606

    Article  Google Scholar 

  • Meynard C, Lopez-Calleja MV, Bozinovic F, Sabat P (1999) Digestive enzymes of a small herbivore, the rufous tailed plant cutter. Condor 101:904–907

    Article  Google Scholar 

  • Naya DE, Ebensperger LA, Sabat P, Bozinovic F (2008) Digestive and metabolic flexibility allows female degus to cope with lactation costs. Physiol Biochem Zool 81:186–194

    Article  PubMed  Google Scholar 

  • Naya DE, Veloso C, Bozinovic F (2009) Gut size variation among Bufo spinulosus populations along an altitudinal (and dietary) gradient. Ann Zool Fenn 46:16–20

    Google Scholar 

  • Ohlson JI, Prum RO, Ericson PGP (2007) A molecular phylogeny of the cotinga (Aves: Cotingidae). Mol Phyl Evol 42:25–37

    Article  CAS  Google Scholar 

  • Penry DL, Jumars PA (1986) Chemical reactor theory and optimal digestion. Bioscience 36:310–315

    Article  CAS  Google Scholar 

  • Pryor GS, Levey DJ, Dierenfeld ES (2001) Protein requirements of a specialized Frugivore, Pesquet’s Parrot (Psittrichas Fulgidus). Auk 118:1080–1088

    Article  Google Scholar 

  • Ramirez-Otarola N, Sabat P (2011) Are levels of digestive enzyme activity related to the natural diet in passerine birds? Biol Res (in press)

  • Renner R, Elcombe AM (1967) Metabolic effects of feeding “carbohydrate free” diets. J Nut 93:31–39

    CAS  Google Scholar 

  • Rohlf FJ (2001) Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55:2143–2160

    PubMed  CAS  Google Scholar 

  • Sabat P (2000) Intestinal disaccharidases and amino-peptidase-N in two species of Cinclodes (Passerine: Furnariidae). Rev Chil Hist Nat 73:345–350

    Google Scholar 

  • Sabat P, Gonzalez SP (2003) Digestive enzymes in two species of marine Cinclodes (Passeriformes: Furnariidae). Condor 105:830–833

    Article  Google Scholar 

  • Sabat P, Veloso C (2003) Ontogenic development of intestinal disaccharidases in the precocial rodent Octodon degus (Octodontidae). Com Biochem Physiol 134:393–397

    Article  Google Scholar 

  • Sabat P, Bozinovic F, Zambrano F (1995) Role of dietary substrates on intestinal disaccharidases digestibility and energetic in the insectivorous mouse-opossum (Thylamys elegans). J Mammal 76:603–611

    Article  Google Scholar 

  • Sabat P, Novoa F, Bozinovic F, Martínez del Rio C (1998) Dietary flexibility and intestinal plasticity in birds: a field and laboratory study. Physiol Zool 71:226–236

    PubMed  CAS  Google Scholar 

  • Sabat P, Lagos JA, Bozinovic F (1999) Test of the adaptive modulation hypothesis in rodents: dietary flexibility and enzyme plasticity. Com Biochem Physiol A 123:83–87

    Article  CAS  Google Scholar 

  • Sabat P, Ramírez-Otarola N, Barceló G, Salinas J, Bozinovic F (2010) Comparative basal metabolic rate among passerines and the food habit hypothesis. Comp Biochem Physiol A 157:35–40

    Google Scholar 

  • Sassi PL, Borghi CE, Bozinovic F (2007) Spatial and seasonal plasticity in digestive morphology of cavies (Microcavia australis) inhabiting habitats with different plant qualities. J Mammal 88:165–172

    Article  Google Scholar 

  • Shondube JE, Martínez del Rio C (2004) Sugar and protein digestion in flowerpiercers and hummingbirds: a comparative test of adaptative convergence. J Com Physiol B 174:263–273

    Article  Google Scholar 

  • Shondube JE, Herrera MLG, Martínez del Rio C (2001) Diet and the evolution of digestion and renal function in phyllostomid bats. Zoology 104:59–73

    Article  Google Scholar 

  • Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds. Yale University Press, New Haven

    Google Scholar 

  • Sibly RM, Calow P (1986) Physiological ecology of animals: an evolutionary approach. Blackwell, Oxford

    Google Scholar 

  • Silva SI, Jaksic FM, Bozinovic F (2005) Nutritional ecology and digestive response to dietary shift in the large South American fox, Pseudalopex culpaeus. Rev Chil Hist Nat 78:239–246

    Google Scholar 

  • Stark JM (2005) Structural flexibility of the digestive system of tetrapods. In: Stark JM, Wang T (eds) Physiological and ecological adaptations to feeding in vertebrates, science. Publishers Inc, New Heaven, pp 175–200

    Google Scholar 

  • Swanson DL, Garland T Jr (2009) The evolution of high summit metabolism and cold tolerance in birds and its impact on present-day distributions. Evolution 63:184–194

    Article  PubMed  CAS  Google Scholar 

  • Tsahar E, Arad Z, Izhaki I, Martínez del Rio C (2006) Do nectar- and fruit-eating birds have lower nitrogen requirements? An allometric test. Auk 123:1004–1012

    Article  Google Scholar 

  • Vonk HJ, Western HR (1984) Comparative biochemistry and physiology of enzymatic digestion. Academic Press, London

    Google Scholar 

  • Weiner J (1992) Physiological limits to sustainable energy budgets in birds and mammals: ecological implications. Trend Ecol Evol 7:384–388

    Article  Google Scholar 

  • Zar JH (1996) Biostatistical analysis. Prentice-Hall, New Jersey

    Google Scholar 

Download references

Acknowledgments

This study was funded by FONDECYT 1080077 to PS. Birds were captured with permits from SAG, Chile (No. 4052/2007). All protocols were approved by the Institutional Animal Care Committee of the Universidad de Chile, where the experiments were performed. We also thank Enrico L. Rezende for his constructive comments on the manuscript.

Author information

Authors and Affiliations

  1. Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile

    Natalia Ramirez-Otarola, Cristóbal Narváez & Pablo Sabat

  2. Center for Advanced Studies in Ecology and Biodiversity, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Casilla 114-D, Santiago, Chile

    Pablo Sabat

Authors
  1. Natalia Ramirez-Otarola
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cristóbal Narváez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pablo Sabat
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pablo Sabat.

Additional information

Communicated by I.D. Hume.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ramirez-Otarola, N., Narváez, C. & Sabat, P. Membrane-bound intestinal enzymes of passerine birds: dietary and phylogenetic correlates. J Comp Physiol B 181, 817–827 (2011). https://doi.org/10.1007/s00360-011-0557-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-011-0557-3

Keywords

Search

Navigation