Advertisement

Journal of Chemical Ecology

, Volume 26, Issue 2, pp 565–584 | Cite as

Habitat-specific Signal Structure for Olfaction: An Example from Artificial Streams

  • Paul A. Moore
  • Jennifer L. Grills
  • Robert W. S. Schneider
Article

Abstract

Many animals use chemical signals to acquire information about their habitats. The structure of this information is dependent upon specific features within a habitat, and the information in signals can be habitat-specific. We quantified the spatial and temporal information in an aquatic odor plume in three different artificial stream habitats with different substrate types by measuring turbulent odor plumes with an electrochemical detection system. Streams had one of three substrate types that correlated with typical aquatic habitats: sand (≈4.2 × 10−2 cm diameter), gravel (≈2.5 cm), and cobble (≈4.5 cm). As predicted from the hydrodynamics, the spatial and temporal structures of the signals were different on different substrates. Spectral analysis showed that the sand and cobble substrates had signals that were dominated by lower frequency fluctuations, whereas gravel had the highest and broadest range of signal fluctuations. Cross- and autocorrelations showed that signals on the gravel substrate had the largest spatial and shortest temporal components. Our results imply that the information obtained from chemical signals may be limited in some habitats. These constraints on information may affect how organisms perform chemically mediated behaviors.

chemoreception fluid dynamics benthic crustaceans stream ecology chemical orientation odor plume chemical signals 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. Aylor, D. E. 1976. Estimating peak concentrations of pheromones in the forest, pp. 177-188, in J. E. Anderson and M. K. Kaya (eds.). Perspectives in Forest Entomology. Academic Press, San Diego, California.Google Scholar
  2. Aylor, D. E., Parlange, Y.-J., and Granett, J. 1976. Turbulent dispersion of disparlure in the forest and male gypsy moth response. Environ. Entomol. 10:211–218.Google Scholar
  3. Bell, W. J., and Tobin, T. R. 1982. Chemo-orientation. Biol. Rev. 57:219–260.Google Scholar
  4. Borroni, P. F., and Atema, J. 1988. Adaptation in chemoreceptor cells I. Self-adapting backgrounds determine threshold and cause parallel shift of dose-response function. J. Comp. Physiol. A 164:67–74.Google Scholar
  5. Borroni, P. F., and Atema, J. 1989. Adaptation in chemoreceptor cells II. The effects of crossadapting backgrounds depend on spectral tuning. J. Comp. Physiol. A 165:669–677.Google Scholar
  6. Bossert, W. H., and Wilson, E. O. 1963. The analysis of olfactory communication among animals. J. Theor. Biol. 5:443–469.Google Scholar
  7. Cheer, A. Y. L., and Koehl, M. A. R. 1987. Paddles and rakes: fluid flow through bristled appendages of small organisms. J. Theor. Biol. 129:17–39.Google Scholar
  8. Devine, D. V., and Atema, J. 1982. Function of chemoreceptor organs in spatial orientation of the lobster Homarus americannus: Differences and overlap. Biol. Bull. 163:144–153.Google Scholar
  9. Gerhardt, G. A., Oke, A. F., Nagy, G., Moghaddam, B., Adams, R. N. 1984. Nafion-coated electrodes with high selectivity for CNS electrochemistry. Brain Res. 290:390–395.Google Scholar
  10. Gifford, F. A. 1968. An outline of theories of diffusion of lower layers of the plume dispersion model. Int. J. Air. Pollut. 3:253–260.Google Scholar
  11. Gleeson, R. A., Carr, W. E. S., and Trapido-Rosenthal, H. G. 1993. Morphological characteristics facilitating stimulus access and removal in the olfactory organ of the spiny lobster Panulirus argus: Insight from design. Chem. Senses 18:67–75.Google Scholar
  12. Gomez, G., Voigt, R., and Atema, J. 1994. Frequency filter properties of lobster chemoreceptor cells determined with high resolution stimulus measurement. J. Comp. Physiol. A 174:803–811.Google Scholar
  13. Hart, D. D., Clark, B. D., and Jasentuliyana, A. 1996. Fine-scale field measurement of benthic flow environments inhabited by stream invertebrates. Limnol. Oceangr. 41:297–308.Google Scholar
  14. Hodgson, E. S., and Matthewson, R. F. 1971. Chemosensory orientation in sharks. Ann. N.Y. Acad. Sci. 188:175–182.Google Scholar
  15. Johnsen, P. B., and Teeter, J. H. 1980. Spatial gradient detection of chemical cues by catfish. J. Comp. Physiol. 140:95–99.Google Scholar
  16. Kennedy, J. S. 1982. Mechanism of moth attraction: a modified view based on wind tunnel experiments with flying male Adoxophyes. Colloq. INRA 7:189–192.Google Scholar
  17. Kundu, P. K. 1990. Fluid Mechanics. Academic Press, New York.Google Scholar
  18. Mafra-Neto, A., and CardÉ, R. T. 1994. Fine-scale structure of pheromone plumes modulates upwind orientation of flying moths. Nature 369:142–144.Google Scholar
  19. Mafra-Neto, A., and CardÉ, R. T. 1995. Influence of plume structure and pheromone concentration on the upwind flight of Cadra cautella males. Physiol. Entomol. 20:117–133.Google Scholar
  20. Mann, K. H., and Lazier, J. R. N. 1996. Dynamics of Marine Ecosystems: Biological-Physical Interactions in the Oceans. Blackwell Science, Cambridge, Massachusetts.Google Scholar
  21. Moore, P. A. 1994. A model of adaptation and disadaptation in olfactory receptor neurons: Implications for the coding of temporal and intensity patterns in odor signals. Chem. Senses 19:71–86.Google Scholar
  22. Moore, P. A., and Atema, J. 1991. Spatial information in the three-dimensional fine structure of an aquatic odor plume. Biol. Bull. 181:408–418.Google Scholar
  23. Moore, P. A., and Grills, J. 1999. Chemical orientation to food by the crayfish, Orconectes rusticus: Influence by hydrodynamics. Anim. Behav. 58:953–963.Google Scholar
  24. Moore, P. A., Gerhardt, G. A., and Atema, J. 1989. High resolution spatio-temporal analysis of aquatic chemical signals using microelectrochemical electrodes. Chem. Senses 14:829–840.Google Scholar
  25. Moore, P. A., Atema, J., and Gerhardt, G. A. 1991a. Fluid dynamics and microscale chemical movement in the chemosensory appendages of the lobster, Homarus americanus. Chem. Senses 16:663–674.Google Scholar
  26. Moore, P. A., Scholz, N., and Atema, J. 1991b. Chemo-orientation of lobsters, Homarus americanus in turbulent odor plumes. J. Chem. Ecol. 17:1293–1307.Google Scholar
  27. Moore, P. A., Weissburg, M. J., Parrish, J. M., Zimmer-Faust, R. K., and Gerhardt, G. A. 1994. Spatial distribution of odors in simulated benthic boundary layer flows. J. Chem. Ecol. 20:255–279.Google Scholar
  28. Murlis, J. 1986. The structure of odour plumes, pp. 27-38, in T. L. Payne, M. C. Birch, and C. E. J. Kennedy (eds.). Mechanisms in Insect Olfaction. Claredon Press, Oxford.Google Scholar
  29. Murlis, J., and Jones, C. D. 1981. Fine-scale structure of odour plumes in relation to insect orientation to distant pheromone and other attractant sources. Physiol. Entomol. 6:71–86.Google Scholar
  30. Nowell, A. R. M., and Jumars, P. A. 1984. Flow environments of aquatic benthos. Annu. Rev. Ecol. Syst. 15:303–328.Google Scholar
  31. Nowell, A. R. M., and Jumars, P. A. 1987. Flumes: Theoretical and experimental considerations for simulation of benthic environments. Oceanogr. Mar. Biol. Annu. Rev. 25:91–112.Google Scholar
  32. Pasquill, F. 1961. The estimation of the disperson of wind-borne material. Meteorol Mag. 90:33–49.Google Scholar
  33. Payne, T. L., Birch, M. C., and Kennedy, C. E. J. (eds.). 1986. Mechanisms in Insect Olfaction. Claredon Press, Oxford.Google Scholar
  34. Peckarsky, B. L. 1980. Predator-prey interactions between stoneflies and mayflies: Behavioral observations. Ecology 61:932–943.Google Scholar
  35. Petranka, J. W., Kats, L. B., and Sih, A. 1987. Predator-prey interaction among fish and larval amphibians: Use of chemical cues to detect prey. Anim. Behav. 35:420–425.Google Scholar
  36. Rubenstein, D. I., and Koehl, M. A. R. 1977. The mechanisms of filter feeding: Some theoretical considerations. Am. Nat. 111:981–994.Google Scholar
  37. Sanford, L. P. 1997. Turbulent mixing in experimental ecosystem studies. Mar. Ecol. Prog. Ser. 161:265–293.Google Scholar
  38. Schlichting, H. 1979. Boundary-Layer Theory, 7th ed. McGraw-Hill, New York.Google Scholar
  39. Schneider, R. W. S., Price, B. A., and Moore, P. A. 1998a. Antennae morphology as a physical filter of olfaction: Temporal tuning of the antennae of the honeybee Apis mellifera. J. Insect Physiol. 44:677–684.Google Scholar
  40. Schneider, R. W. S., Lanzen, J., and Moore, P. A. 1998b. Boundary layer effect on chemical signal movement near the antennae of the Sphinx moth Manduca sexta: Temporal filters for olfaction. J. Comp. Physiol. A 182:287–305.Google Scholar
  41. Suckling, D. M., and Karg, G. 1997. The role of foliage on mating disruption in apple orchards. Technology transfer in mating disruption. IOBC WPRS Bull. 20:169–174.Google Scholar
  42. Suckling, D. M., Karg, G., and Bradley, S. J. 1996. Apple foliage enhances mating disruption of lightbrown apple moth. J. Chem. Ecol. 22:325–341.Google Scholar
  43. Sutton, O. G. 1953. Micrometeorology. McGraw-Hill, New York.Google Scholar
  44. Tennekes, H., and Lumley, J. L. 1972. A First Course in Turbulence. MIT Press, Cambridge, Massachusetts.Google Scholar
  45. Vickers, N. J., and Baker, T. C. 1992. Male Heliothis virescens maintain upwind flight in response to experimentally pulsed filaments of their sex pheromone (Lepidoptera: Noctuidae). J. Insect Behav. 5:669–687.Google Scholar
  46. Vickers, N. J., and Baker, T. C. 1994. Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths. Proc. Natl. Acad. Sci. U.S.A. 91:5756–5760.Google Scholar
  47. Weissburg, M. J., and Zimmer-Faust, R. K. 1993. Life and death in moving fluids: Hydrodynamic effects on chemosensory-mediated predation. Ecology 74:1428–1443.Google Scholar
  48. Westerberg, H. 1991. Properties of aquatic odour trails, pp. 45-65, in K. Dø ving (ed.). Proceedings of the Tenth International Symposium on Olfaction and Taste. Graphic Communication System, Oslo.Google Scholar
  49. Zimmer-Faust, R. K., Sanfill, J. M., and Collard III, S. B. 1988. A fast multichannel fluorometer for investigating aquatic chemoreception and odor trails. Limnol. Oceanogr. 33:1586–1595.Google Scholar

Copyright information

© Plenum Publishing Corporation 2000

Authors and Affiliations

  • Paul A. Moore
    • 1
    • 2
  • Jennifer L. Grills
    • 1
    • 2
  • Robert W. S. Schneider
    • 1
    • 2
  1. 1.Laboratory for Sensory Ecology, Department of Biological SciencesBowling Green State UniversityBowling Green
  2. 2.University of Michigan Biological StationPellston

Personalised recommendations