Advertisement

Marine Biology

, Volume 151, Issue 4, pp 1551–1558 | Cite as

A comparison of absorption and assimilation efficiencies between four species of shallow- and deep-living fishes

  • Jeffrey C. Drazen
  • Kim R. Reisenbichler
  • Bruce H. Robison
Research Article

Abstract

We captured two species of deep-sea zoarcids, Melanostigma pammelas and Lycodapus mandibularis, from Monterey Bay California and maintained them in the laboratory. One shallow-water zoarcid, Eucryphycus californicus, and an ecologically and morphologically similar stichaeid fish Xiphister atropurpureus were collected from intertidal and subtidal habitats in Monterey Bay. We investigated the absorption and assimilation efficiencies of these fishes to determine whether deep-sea species have evolved mechanisms to increase their efficiency of food use. Fishes were placed in experimental chambers and fed a known quantity of food. Ammonia excretion was measured and feces were collected daily. Both food and feces were analyzed for water, protein, lipid and ash to determine specific absorption efficiencies. Absorption ranged from 87.7 to 92.4% and assimilation efficiencies from 84.0 to 86.5%. Meal sizes from 0.5 to 4.0% of body weight did not affect the results. No significant differences were found between deep-sea and shallow-water species fed single meals or fed ad libitum for 10 days. This suggests that the selective pressure to maximize absorption and assimilation is universal and is not affected by the productivity of the habitat occupied. However, the relative size of the intestine in the deep-sea species was significantly smaller suggesting that they had a lower metabolic cost to maintain their digestive apparatus. It could not be concluded whether this was the result of pressure to conserve energy or rather the tendency of the shallow-living species to ingest more refractory material (i.e. sediment, algae).

Keywords

Absorption Efficiency Assimilation Efficiency Meal Size Meal Frequency Single Meal 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank Tonatiuh Trejo and Magdalena Gutowska for help with initial experiments in the lab. Steve Haddock kindly allowed us to use his seawater lab. Thanks to Greg Cailliet and Lara Ferry-Graham for collecting some of the E. californica and to Joe Welsh and John O’Sullivan for help collecting the X. atropurpureus. Chris Wood and Danielle McDonald (McMaster University) provided detailed protocols and advice for measuring ammonia and urea. J. Drazen was supported by a MBARI postdoctoral fellowship. Supported by the David and Lucile Packard Foundation.

References

  1. Anderson ME (1980) Aspects of the natural history of the midwater fish Lycodapus mandibularis (Zoarcidae) in Monterey Bay, California. Pac Sci 34:181–194Google Scholar
  2. Angel MV, Baker AC (1982) Vertical distribution of the standing crop of plankton and micronekton at three stations in the northeast Atlantic. Biol Oceanogr 2:1–30Google Scholar
  3. Barton MG (1982) Intertidal vertical distribution and diets of five species of central California stichaeoid fishes. Calif Fish Game 68:174–182Google Scholar
  4. Benavides AG, Cancino JM, Ojeda FP (1994) Ontogenetic changes in gut dimensions and macroalgal digestibility in the marine herbivorous fish, Aplodactylus punctatus. Funct Ecol 8:46–51CrossRefGoogle Scholar
  5. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917CrossRefGoogle Scholar
  6. Brafield AE (1985) Laboratory studies of energy budgets. In: Tytler P, Calow P (eds) Fish energetics: new perspectives. The John Hopkins University Press, Baltimore, pp 257–282CrossRefGoogle Scholar
  7. Brett JR, Groves TDD (1979) Physiological energetics. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol. 8. Bioenergetics and growth. Academic, New York, pp 280–352Google Scholar
  8. Cailliet GM, Lea RN (1977) Abundance of the ‘rare’ zoarcid, Maynea californica Gilbert, 1915, in the Monterey Canyon, Monterey Bay, California. Calif Fish Game 63:253–261Google Scholar
  9. Chan AS, Horn MH, Dickson KA, Gawlicka A (2004) Digestive enzyme activities in carnivores and herbivores: comparisons among four closely related prickleback fishes (Teleostei: Stichaeidae) from a California rocky intertidal habitat. J Fish Biol 65:848–858CrossRefGoogle Scholar
  10. Childress JJ (1971) Respiratory rate and depth of occurrence of midwater animals. Limnol Oceanogr 16:104–106CrossRefGoogle Scholar
  11. Childress JJ (1995) Are there physiological and biochemical adaptations of metabolism in deep-sea animals? Trends Ecol Evol 10:30–36CrossRefGoogle Scholar
  12. Childress JJ, Cowles DL, Favuzzi JA, Mickel TJ (1990) Metabolic rates of benthic deep-sea decapod crustaceans decline with increasing depth primarily due to the decline in temperature. Deep Sea Res 37:929–949CrossRefGoogle Scholar
  13. Cho CY, Slinger SJ, Bayley HS (1982) Bioenergetics of salmonid fishes: energy intake, expenditure and productivity. Comp Biochem Physiol 73B:25–41Google Scholar
  14. Choubert G (1999) Nutrient digestibility in fish: methodological aspects. Cybium 23(suppl):113–125Google Scholar
  15. Cleveland A, Montgomery WL (2003) Gut characteristics and assimilation efficiencies in two species of herbivorous damselfishes (Pomacentridae: Stegastes dorsopunicans and S. planifrons). Mar Biol 142:35–44CrossRefGoogle Scholar
  16. Collins MA, Priede IG, Bagley PM (1999) In situ comparison of activity in two deep-sea scavenging fishes occupying different depth zones. Proc R Soc Lond B 266:2011–2016CrossRefGoogle Scholar
  17. Eastman JT, DeVries AL (1997) Morphology of the digestive system of Antarctic nototheniid fishes. Polar Biol 17:1–13CrossRefGoogle Scholar
  18. Fänge R, Grove D (1979) Digestion. In: Hoar WS, Randall DJ, Brett JR (eds) Fish physiology, vol. 8. Bioenergetics and growth. Academic, New York, pp 161–260Google Scholar
  19. Ferry-Graham LA, Drazen JC, Franklin V (2007) Laboratory observations of reproduction in deep-water zoarcids (Teleostei). Pac Sci 61:129–139CrossRefGoogle Scholar
  20. German D, Horn M (2006) Gut length and mass in herbivorous and carnivorous prickleback fishes (Teleostei: Stichaeidae): ontogenetic, dietary, and phylogenetic effects. Mar Biol 148:1123CrossRefGoogle Scholar
  21. Gutowska MA, Drazen JC, Robison BH (2004) Digestive chitinolytic activity in marine fishes of Monterey Bay, California. Comp Biochem Physiol A 139:351–358CrossRefGoogle Scholar
  22. Haedrich RL, Rowe GT (1977) Megafaunal biomass in the deep sea. Nature 269:141–142CrossRefGoogle Scholar
  23. Haedrich RL, Rowe GT, Polloni PT (1980) The megabenthic fauna in the deep sea south of New England, USA. Mar Biol 57:165–179CrossRefGoogle Scholar
  24. Hargrave BT, Phillips GA, Prouse NJ, Cranford PJ (1995) Rapid digestion and assimilation of bait by the deep-sea amphipod Eurythenes gryllus. Deep Sea Res I 42:1905CrossRefGoogle Scholar
  25. Herring PJ (2002) The biology of the deep ocean. Oxford University Press, OxfordGoogle Scholar
  26. Horn MH (1989) Biology of marine herbivorous fishes. Oceanogr Mar Biol Annu Rev 27:167–272Google Scholar
  27. Ivancic I, Degobbis D (1984) An optimal manual procedure for ammonia analysis in natural waters by the indophenol blue method. Water Res 18:1143–1147CrossRefGoogle Scholar
  28. Jobling M (1993) Bioenergetics: feed intake and energy partitioning. In: Rankin JC, Jensen FB (eds) Fish ecophysiology. Chapman & Hall, London, pp 1–44Google Scholar
  29. Kapoor BG, Smit H, Verighina IA (1975) The alimentary canal and digestion in teleosts. Adv Mar Biol 13: 109–239CrossRefGoogle Scholar
  30. Kliever RG (1976) Natural history of Maynea californica (Pisces: Zoarcidae) in a drift seaweed habitat in the Monterey Submarine Canyon, Monterey Bay, California. M.S. San Jose State University, San JoseGoogle Scholar
  31. 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 42:129–141CrossRefGoogle Scholar
  32. Lampitt RS, Billett DSM, Rice AL (1986) Biomass of the invertebrate megabenthos from 500 to 4100 m in the Northeast Atlantic Ocean. Mar Biol 93:69–81CrossRefGoogle Scholar
  33. Lancraft TM (1982) Aspects of the natural history of Melanostigma pammelas (Pisces: Zoarcidae). MA thesis. University of California, Santa BarbaraGoogle Scholar
  34. Marsh JB, Weinstein DB (1966) Simple charring method for determination of lipids. J Lipid Res 7:574–576PubMedGoogle Scholar
  35. Marshall NB (1954) Aspects of deep-sea biology. Philosophical Library, New YorkGoogle Scholar
  36. McAllister DE (1961) A collection of oceanic fishes from off British Columbia with a discussion of the evolution of the black peritoneum. Bull Natl Mus Can, Contrib Zool 172:39–43Google Scholar
  37. Merrett N, Haedrich RL (1997) Deep-sea demersal fish and fisheries. Chapman & Hall, LondonGoogle Scholar
  38. Pandian TJ, Vivekanandan E (1985) Energetics of feeding and digestion. In: Tytler P, Calow P (eds) Fish energetics: new perspectives. The John Hopkins University Press, Baltimore, pp 99–124CrossRefGoogle Scholar
  39. Penry DL, Jumars PA (1987) Modeling animal guts as chemical reactors. Am Nat 129:69–96CrossRefGoogle Scholar
  40. Penry DL, Jumars PA (1990) Gut architecture, digestive constraints and feeding ecology of deposit-feeding and carnivorous polychaetes. Oecologia 82:1–11CrossRefGoogle Scholar
  41. Price NM, Harrison PJ (1987) Comparison of methods for the analysis of dissolved urea in seawater. Mar Biol 94:307–317CrossRefGoogle Scholar
  42. Priede IG, Deary AR, Bailey DM, Smith KL Jr. (2003) Low activity and seasonal change in population size structure of grenadiers in the oligotrophic abyssal central North Pacific Ocean. J Fish Biol 63:187–196CrossRefGoogle Scholar
  43. Reisenbichler KR, Bailey TG (1991) Microextraction of total lipid from mesopelagic animals. Deep Sea Res 38:1331–1339CrossRefGoogle Scholar
  44. Robison BH (1984) Herbivory by the myctophid fish Ceratoscopelus warmingii. Mar Biol 84:119–123CrossRefGoogle Scholar
  45. Robison BH (2004) Deep pelagic biology. J Exp Mar Biol Ecol 300:253–272CrossRefGoogle Scholar
  46. Robison BH, Bailey TG (1981) Nutrient energy flux in midwater fishes. In: Cailliet G, Simenstad CA (eds) Pacific northwest technical workshop, gutshop 81. Washington Seagrant, Pacific Grove, pp 80–87Google Scholar
  47. Seibel BA, Drazen JC (2006) The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities. Philos Trans R Soc Lond, B 362 (in press)CrossRefGoogle Scholar
  48. Sibly RM, Calow P (1986) Physiological ecology of animals. Blackwell Scientific Publications, OxfordGoogle Scholar
  49. Smith KL Jr, Hessler RR (1974) Respiration of benthopelagic fishes: in situ measurements at 1230 meters. Science 184:72–73CrossRefGoogle Scholar
  50. Smith PL, Krohn RL, Hermanson GT, Mallia AK, Gartner MD, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85CrossRefGoogle Scholar
  51. Vandenberg G, De La nouee J (2001) Apparent digestibility comparison in rainbow trout (Oncorhynchus mykiss) assessed using three methods of faeces collection and three digestibility markers. Aquac Nutr 7:237–245CrossRefGoogle Scholar
  52. Young RE (1983) Oceanic bioluminescence: an overview of general functions. Bull Mar Sci 33:829–845Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Jeffrey C. Drazen
    • 1
  • Kim R. Reisenbichler
    • 2
  • Bruce H. Robison
    • 2
  1. 1.Department of OceanographyUniversity of HawaiiHonoluluUSA
  2. 2.Monterey Bay Aquarium Research InstituteMoss LandingUSA

Personalised recommendations