Skip to main content

Changes in digestive traits and body nutritional composition accommodate a trophic niche shift in Trinidadian guppies

Abstract

A trophic niche shift can occur as an adaptive response to environmental change such as altered resource quality, abundance or composition. Alterations in digestive traits such as gut morphology and physiology may enable these niche shifts and affect the persistence of populations and species. Relatively few studies, however, have assessed how niche shifts influence suites of digestive traits through phenotypic plasticity and evolutionary mechanisms, and how these trait changes can subsequently alter the nutrition, fitness and life history of organisms. We investigated how population divergence and plasticity alter the gut physiology of wild Trinidadian guppies (Poecilia reticulata), assessing whether variation in digestive traits correspond with enhanced nutrient assimilation under a pronounced dietary shift. We examined gut enzyme activity, and gut size and mass of wild guppies from both high-predation (HP) and low-predation (LP) habitats when reared in the laboratory and fed on high- or low-quality diets designed to reflect their dietary differences previously found in nature. After 10 weeks on the experimental diets, HP guppies maintained shorter and lighter guts than LP guppies on either diet. Guppies also differed in their digestive enzymatic profiles, more often reflecting nutrient balancing so that increased enzyme expression tended to correspond with more deficient nutrients in the diet. LP guppies had increased somatic phosphorus at the end of the experiment, possibly related to the higher alkaline phosphatase activity in their guts. Our results suggest that differences in gut physiology exist among populations of Trinidadian guppies that may reflect local adaptation to their disparate environments.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Arendt J, Reznick D (2005) Evolution of juvenile growth rates in female guppies (Poecilia reticulata): predator regime or resource level? Proc R Soc Lond B 272:333–337

    Article  Google Scholar 

  2. Arendt JD, Reznick DN, López-Sepulcre A (2014) Replicated origin of female biased adult sex ratio in introduced populations of the Trinidadian guppy (Poecilia reticulata). Evolution. doi:10.1111/evo.12445

    PubMed  Google Scholar 

  3. Auer SK, Arendt JD, Chandramouli R, Reznick DN (2010) Juvenile compensatory growth has negative consequences for reproduction in Trinidadian guppies (Poecilia reticulata). Ecol Lett 13:998–1007. doi:10.1111/j.1461-0248.2010.01491.x

    PubMed  Google Scholar 

  4. Baeverfjord G, Åsgård T, Shearer KD (1998) Development and detection of phosphorus deficiency in Atlantic salmon, Salmo salar L., parr and post-smolts. Aquac Nutr 4:1–11. doi:10.1046/j.1365-2095.1998.00095.x

    CAS  Article  Google Scholar 

  5. Bassar RD et al (2010) Local adaptation in Trinidadian guppies alters ecosystem processes. Proc Natl Acad Sci USA 107:3616–3621. doi:10.1073/pnas.0908023107

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  6. Bates JM, Akerlund J, Mittge E, Guillemin K (2007) Intestinal alkaline phosphatase detoxifies lipopolysaccharide and prevents inflammation in zebrafish in response to the gut microbiota. Cell Host Microbe 2:371–382

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  7. Brown JH, Gupta VK, Li B-L, Milne BT, Restrepo C, West GB (2002) The fractal nature of nature: power laws, ecological complexity and biodiversity. Philos Trans R Soc Lond B 357:619–626. doi:10.1098/rstb.2001.0993

    Article  Google Scholar 

  8. Cant JP, McBride BW, Croom WJ (1996) The regulation of intestinal metabolism and its impact on whole animal energetics. J Anim Sci 74:2541–2553

    CAS  PubMed  Google Scholar 

  9. Caviedes-Vidal E, Afik D, Martinez del Rio C, Karasov WH (2000) Dietary modulation of intestinal enzymes of the house sparrow (Passer domesticus): testing an adaptive hypothesis. Comp Biochem Physiol A 125:11–24. doi:10.1016/S1095-6433(99)00163-4

    CAS  Article  Google Scholar 

  10. Charo-Karisa H, Bovenhuis H, Rezk MA, Ponzoni RW, van Arendonk JAM, Komen H (2007) Phenotypic and genetic parameters for body measurements, reproductive traits and gut length of Nile tilapia (Oreochromis niloticus) selected for growth in low-input earthen ponds. Aquaculture 273:15–23. doi:10.1016/j.aquaculture.2007.09.011

    Article  Google Scholar 

  11. Clements KD, Raubenheimer D (2006) Feeding and nutrition. In: Evans DH, Claiborne JB (eds) The physiology of fishes. CRC, Boca Raton

    Google Scholar 

  12. Clissold FJ, Tedder BJ, Conigrave AD, Simpson SJ (2010) The gastrointestinal tract as a nutrient-balancing organ. Proc R Soc Lond B 277:1751–1759. doi:10.1098/rspb.2009.2045

    Article  Google Scholar 

  13. Dabrowski K, Glogowski J (1977) Studies on the role of exogenous proteolytic enzymes in digestion processes in fish. Hydrobiologia 54:129–134. doi:10.1007/bf00034986

    CAS  Article  Google Scholar 

  14. Day R, German D, Manjakasy J, Farr I, Hansen M, Tibbetts I (2011) Enzymatic digestion in stomachless fishes: how a simple gut accommodates both herbivory and carnivory. J Comp Physiol B 181:603–613. doi:10.1007/s00360-010-0546-y

    CAS  PubMed  Article  Google Scholar 

  15. Demott WR, Gulati RD, Siewertsen K (1998) Effects of phosphorus-deficient diets on the carbon and phosphorus balance of Daphnia magna. Limnol Oceanogr 43:1147–1161

    CAS  Article  Google Scholar 

  16. El-Sabaawi RW et al (2012) Widespread intraspecific organismal stoichiometry among populations of the Trinidadian guppy. Funct Ecol 26:666–676. doi:10.1111/j.1365-2435.2012.01974.x

    Article  Google Scholar 

  17. Elser JJ et al (2000) Nutritional constraints in terrestrial and freshwater foodwebs. Nature 408:578–580. doi:10.1038/35046058

    CAS  PubMed  Article  Google Scholar 

  18. Fraser DF, Gilliam JF (1992) Nonlethal impacts of predator invasion: facultative suppression of growth and reproduction. Ecology 73:959–970. doi:10.2307/1940172

    Article  Google Scholar 

  19. Fraser DF, Gilliam JF, Akkara JT, Albanese BW, Snider SB (2004) Night feeding by guppies under predator release: effects on growth and daytime courtship. Ecology 85:312–319. doi:10.2307/3450197

    Article  Google Scholar 

  20. Frost P, Ebert D, Larson J, Marcus M, Wagner N, Zalewski A (2010) Transgenerational effects of poor elemental food quality on Daphnia magna. Oecologia 162:865–872. doi:10.1007/s00442-009-1517-4

    PubMed  Article  Google Scholar 

  21. German DP, Horn MH (2006) Gut length and mass in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Mar Biol 148:1123–1134. doi:10.1007/s00227-005-0149-4

    Article  Google Scholar 

  22. German DP, Horn MH, Gawlicka A (2004) Digestive enzyme activities in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Physiol Biochem Zool 77:789–804. doi:10.1086/422228

    CAS  PubMed  Article  Google Scholar 

  23. German DP et al (2010) Evolution of herbivory in a carnivorous clade of minnows (Teleostei: Cyprinidae): effects on gut size and digestive physiology. Physiol Biochem Zool 83:1–18. doi:10.1086/648510

    PubMed  Article  Google Scholar 

  24. German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43:1387–1397. doi:10.1016/j.soilbio.2011.03.017

    CAS  Article  Google Scholar 

  25. German DP, Gawlicka AK, Horn MH (2014) Evolution of ontogenetic dietary shifts and associated gut features in prickleback fishes (Teleostei: Stichaeidae). Comp Biochem Physiol B 168:12–18. doi:10.1016/j.cbpb.2013.11.006

    CAS  PubMed  Article  Google Scholar 

  26. Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407. doi:10.1111/j.1365-2435.2007.01283.x

    Article  Google Scholar 

  27. Grant PR, Grant BR (2006) Evolution of character displacement in Darwin’s finches. Science 313:224–226. doi:10.1126/science.1128374

    CAS  PubMed  Article  Google Scholar 

  28. Grether GF, Millie DF, Bryant MJ, Reznick DN, Mayea W (2001) Rain forest canopy cover, resource availability, and life history evolution in guppies. Ecology 82:1546–1559

    Article  Google Scholar 

  29. Hakim Y, Uni Z, Hulata G, Harpaz S (2006) Relationship between intestinal brush border enzymatic activity and growth rate in tilapias fed diets containing 30 or 48 % protein. Aquaculture 257:420–428. doi:10.1016/j.aquaculture.2006.02.034

    CAS  Article  Google Scholar 

  30. Harpaz S, Uni Z (1999) Activity of intestinal mucosal brush border membrane enzymes in relation to the feeding habits of three aquaculture fish species. Comp Biochem Physiol A 124:155–160. doi:10.1016/S1095-6433(99)00106-3

    Article  Google Scholar 

  31. Hendrixson HA, Sterner RW, Kay AD (2007) Elemental stoichiometry of freshwater fishes in relation to phylogeny, allometry and ecology. J Fish Biol 70:121–140. doi:10.1111/j.1095-8649.2006.01280.x

    Article  Google Scholar 

  32. Horn MH (1989) Biology of marine herbivorous fishes. Oceanogr Mar Biol Annu Rev 27:167–272

    Google Scholar 

  33. Horn MH, Gawlicka AK, German DP, Logothetis EA, Cavanagh JW, Boyle KS (2006) Structure and function of the stomachless digestive system in three related species of new world silverside fishes (Atherinopsidae) representing herbivory, omnivory, and carnivory. Mar Biol 149:1237–1245. doi:10.1007/s00227-006-0281-9

    Article  Google Scholar 

  34. Karasov WH, Hume ID (1997) The vertebrate gastrointestinal system. In: Dantzler WH (ed) Handbook of physiology, Section 13: comparative physiology, vol 1. Oxford University Press, New York, pp 407–480

    Google Scholar 

  35. Karasov WH, Martinez del Rio C (2007) Physiological ecology: how animals process energy, nutrients, and toxins. Princeton University Press, Princeton

    Google Scholar 

  36. Karasov WH, Martínez del Rio C, Caviedes-Vidal E (2011) Ecological physiology of diet and digestive systems. Annu Rev Physiol 73:69–93. doi:10.1146/annurev-physiol-012110-142152

    CAS  PubMed  Article  Google Scholar 

  37. Ketola HG, Richmond ME (1994) Requirement of rainbow trout for dietary phosphorus and its relationship to the amount discharged in hatchery effluents. Trans Am Fish Soc 123:587–594. doi:10.1577/1548-8659(1994)123<0587:rortfd>2.3.co;2

    CAS  Article  Google Scholar 

  38. Koch AL (1985) The macroeconomics of bacterial growth. In: Fletcher M, Floodgate GD (eds) Bacteria in their natural environments. Academic, London, pp 1–42

    Google Scholar 

  39. Kramer DL, Bryant MJ (1995) Intestine length in the fishes of a tropical stream: 2. Relationships to diet–the long and short of a convoluted issue. Environ Biol Fish 42:129–141. doi:10.1007/BF00001991

    Article  Google Scholar 

  40. Lallès JP (2010) Intestinal alkaline phosphatase: multiple biological roles in maintenance of intestinal homeostasis and modulation by diet. Nutr Rev 68:323–332. doi:10.1111/j.1753-4887.2010.00292.x

    PubMed  Article  Google Scholar 

  41. Magurran AE (2005) Evolutionary ecology: The Trinidadian guppy. Oxford University Press, New York

    Book  Google Scholar 

  42. Matthews B et al (2011) Toward an integration of evolutionary biology and ecosystem science. Ecol Lett 14:690–701. doi:10.1111/j.1461-0248.2011.01627.x

    PubMed  Article  Google Scholar 

  43. McCarthy SDS, Rafferty SP, Frost PC (2010) Responses of alkaline phosphatase activity to phosphorus stress in Daphnia magna. J Exp Biol 213:256–261. doi:10.1242/jeb.037788

    CAS  PubMed  Article  Google Scholar 

  44. McIntyre PB, Flecker AS, Vanni MJ, Hood JM, Taylor BW, Thomas SA (2008) Fish distributions and nutrient cycling in streams: can fish create biogeochemical hotspots? Ecology 89:2335–2346. doi:10.1890/07-1552.1

    PubMed  Article  Google Scholar 

  45. Palkovacs EP, Kinnison MT, Correa C, Dalton CM, Hendry AP (2012) Fates beyond traits: ecological consequences of human-induced trait change. Evol Appl 5:183–191. doi:10.1111/j.1752-4571.2011.00212.x

    PubMed Central  Article  Google Scholar 

  46. Parsons KJ, Robinson BW (2007) Foraging performance of diet-induced morphotypes in pumpkinseed sunfish (Lepomis gibbosus) favours resource polymorphism. J Evol Biol 20:673–684. doi:10.1111/j.1420-9101.2006.01249.x

    CAS  PubMed  Article  Google Scholar 

  47. Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis, 1st edn. Pergamon, New York

    Google Scholar 

  48. Poelstra K, Bakker WW, Klok PA, Hardonk MJ, Meijer DK (1997) A physiologic function for alkaline phosphatase: endotoxin detoxification. Lab Invest 76:319–327

    CAS  PubMed  Google Scholar 

  49. R Development Core Team (2012) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for statistical computing. See http://www.r-project.org/

  50. Relyea RA, Auld JR (2004) Having the guts to compete: how intestinal plasticity explains costs of inducible defences. Ecol Lett 7:869–875. doi:10.1111/j.1461-0248.2004.00645.x

    Article  Google Scholar 

  51. Reznick D (1982) The impact of predation on life history evolution in Trinidadian guppies: genetic basis of observed life history patterns. Evolution 36:1236–1250. doi:10.2307/2408156

    Article  Google Scholar 

  52. Reznick DN (1983) The structure of guppy life histories: the tradeoff between growth and reproduction. Ecology 64:862–873

    Article  Google Scholar 

  53. Rodd FH, Reznick DN (1997) Variation in the demography of guppy populations: the importance of predation and life histories. Ecology 78:405–418. doi:10.2307/2266017

    Google Scholar 

  54. Schluter D (1995) Adaptive radiation in sticklebacks: trade-offs in feeding performance and growth. Ecology 76:82–90. doi:10.2307/1940633

    Article  Google Scholar 

  55. Sibly RM (1981) Strategies of digestion and defecation. In: Townsend CR, Calow P (eds) Physiological ecology: an evolutionary approach to resource use. Blackwell, Oxford, pp 109–139

    Google Scholar 

  56. Sterner JW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  57. Stevens CE, Hume ID (1995) Comparative physiology of the vertebrate digestive system. Cambridge University Press, Cambridge

    Google Scholar 

  58. Taylor BW, Flecker AS, Hall RO (2006) Loss of a harvested fish species disrupts carbon flow in a diverse tropical river. Science 313:833–836. doi:10.1126/science.1128223

    CAS  PubMed  Article  Google Scholar 

  59. Thomas CD et al (2004) Extinction risk from climate change. Nature 427:145–148. doi:10.1038/nature02121

    CAS  PubMed  Article  Google Scholar 

  60. Torres LE, Vanni MJ (2007) Stoichiometry of nutrient excretion by fish: interspecific variation in a hypereutrophic lake. Oikos 116:259–270. doi:10.1111/j.0030-1299.2007.15268.x

    CAS  Article  Google Scholar 

  61. Torres-Dowdall J, Handelsman CA, Reznick DN, Ghalambor CK (2012) Local adaptation and the evolution of phenotypic plasticity in Trinidadian guppies (Poecilia reticulata). Evolution 66:3432–3443. doi:10.1111/j.1558-5646.2012.01694.x

    PubMed  Article  Google Scholar 

  62. Tracy CR, Diamond J (2005) Regulation of gut function varies with life history traits in Chuckwallas (Sauromalus obesus: Iguanidae). Physiol Biochem Zool 78:469–481

    PubMed  Article  Google Scholar 

  63. Wagner CE, McIntyre PB, Buels KS, Gilbert DM, Michel E (2009) Diet predicts intestine length in Lake Tanganyika’s cichlid fishes. Funct Ecol 23:1122–1131. doi:10.1111/j.1365-2435.2009.01589.x

    Article  Google Scholar 

  64. Werner EE, Gilliam JF, Hall DJ, Mittelbach GG (1983) An experimental test of the effects of predation risk on habitat use in fish. Ecology 64:1540–1548. doi:10.2307/1937508

    Article  Google Scholar 

  65. Zandonà E (2010) The trophic ecology of guppies (Poecilia reticulata) from the streams of Trinidad. PhD thesis, Drexel University, Philadelphia

  66. Zandonà E et al (2011) Diet quality and prey selectivity correlate with life histories and predation regime in Trinidadian guppies. Funct Ecol 25:964–973. doi:10.1111/j.1365-2435.2011.01865.x

    Article  Google Scholar 

  67. Zemke-White WL, Clements KD (1999) Chlorophyte and rhodophyte starches as factors in diet choice by marine herbivorous fish. J Exp Mar Biol Ecol 240:137–149. doi:10.1016/S0022-0981(99)00056-8

    Article  Google Scholar 

Download references

Acknowledgments

This work was funded, in part, by the National Science Foundation, Frontiers in Integrative Biological Research Guppy Project (DEB-0623632EF). The L.D. Betz Chair of Environmental Science contributed funds to this project as well as the James H. Glass and the Elihu Root Fellowships awarded to K.E.S. from Hamilton College. We thank Eugenia Zandonà, David Reznick, Michael O’Connor and Blake Matthews for discussions about the research, Amy McCune for sharing her laboratory space, and Mauri Ren for laboratory assistance. We also thank the handling editor and 2 anonymous reviewers whose comments improved this manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Karen E. Sullam.

Additional information

K. E. Sullam, C. M. Dalton contributed equally.

Communicated by Ken Spitze.

Electronic supplementary material

Supplementary Figures S1–S2, Tables S1–S14, and text with additional details regarding experimental set-up and results of body composition analysis are included in Electronic Supplementary Material. Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 795 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sullam, K.E., Dalton, C.M., Russell, J.A. et al. Changes in digestive traits and body nutritional composition accommodate a trophic niche shift in Trinidadian guppies. Oecologia 177, 245–257 (2015). https://doi.org/10.1007/s00442-014-3158-5

Download citation

Keywords

  • Digestive enzymes
  • Gut morphology
  • Local adaptation
  • Nutrient balancing
  • Poecilia
  • Stoichiometry