Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-13T03:41:04.516Z Has data issue: false hasContentIssue false

Egg mass ventilation by caridean shrimp: similarities to other decapods and insight into pheromone receptor location

Published online by Cambridge University Press:  24 March 2014

Kathleen A. Reinsel*
Affiliation:
Department of Biology, Wittenberg University, Springfield, OH 45502USA
Kerry Pagel
Affiliation:
Department of Biology, Wittenberg University, Springfield, OH 45502USA
Margaret Kissel
Affiliation:
Duke University Marine Laboratory, Beaufort, NC 28516USA
Erin Foran
Affiliation:
Duke University Marine Laboratory, Beaufort, NC 28516USA
Anthony S. Clare
Affiliation:
School of Marine Science and Technology, Armstrong Building, Newcastle University, Newcastle upon Tyne NE1 7RU, UK
Dan Rittschof
Affiliation:
Duke University Marine Laboratory, Beaufort, NC 28516USA
*
Correspondence should be addressed to: K.A. Reinsel, Department of Biology, Wittenberg University, Springfield, OH 45502USA email: kreinsel@wittenberg.edu

Abstract

Egg clutch brooding and larval release behaviour are common among decapods and involve pheromone communication between the developing embryos and the brooding female. We tested caridean shrimps to determine whether their behaviour was similar to other decapods. In tests with aqueous extracts of crushed eggs and peptide pheromone mimic shrimps responded similarly to brachyurans and lobsters. The elongate body form of shrimps enabled us to focally stimulate body locations with the goal of determining the location of pheromone receptors. The receptors for the pheromones are likely located on the bases of the walking legs or on the gills, not on the pleopods, first walking legs, antennae or antennules. Shrimps are another example of organisms that use peptides generated by trypsin-like serine proteases as pheromones and signal molecules.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ache, B.W. and McClintock, T. (1990) The lobster olfactory receptor cell as a neurobiological model: the action of histamine. Frontiers in Crustacean Neurobiology 33, 3339.Google Scholar
Atema, J. and Cowan, D. (1986) Sex-identifying urine and molt signals in lobster (Homarus americanus). Journal of Chemical Ecology 12, 20652080.Google Scholar
Baeza, J.A. and Fernández, M. (2002) Active brood care in Cancer setosus (Crustacea: Decapoda): the relationship between female behaviour, embryo oxygen consumption and the cost of brooding. Functional Ecology 16, 241251.Google Scholar
Bauer, R.T. (1979) Antifouling adaptations of marine shrimp (Decapoda: Caridea): gill cleaning mechanisms and grooming of brooded embryos. Zoological Journal of the Linnean Society 65, 281303.Google Scholar
Branford, J.R. (1978) The influence of daylength, temperature and season on the hatching rhythm of Homarus gammarus. Journal of the Marine Biological Association of the United Kingdom 58, 639658.Google Scholar
Brooks, W.R., Ceperley, L. and Rittschof, D. (1995) Disturbance and reattachment behaviour of sea anemones Calliactis tricolor (Le Sueur): temporal, textural and chemical mediation. Journal of Chemical Ecology 21, 112.Google Scholar
Cheung, T.S. (1966) The development of egg-membranes and egg attachment in the shore crab, Carcinus maenas, and some related decapods. Journal of the Marine Biological Association of the United Kingdom 46, 373400.Google Scholar
Darnell, M.Z. and Rittschof, D. (2010) Role of larval release pheromones and peptide mimics in abdominal pumping and swimming behaviour of ovigerous blue crabs, Callinectes sapidus. Journal of Experimental Marine Biology and Ecology 391, 112117.CrossRefGoogle Scholar
De Vries, M.C. and Forward, R.B. Jr (1991a) Control of egg-hatching time in crabs from different tidal heights. Journal of Crustacean Biology 11, 2939.Google Scholar
De Vries, M.C. and Forward, R.B. Jr (1991b) Mechanisms of crustacean egg hatching: Evidence for enzyme release by crab embryos. Marine Biology 110, 281291.Google Scholar
De Vries, M.C., Rittschof, D. and Forward, R.B. Jr (1989) Response by Rhizocephalan-parasitized crabs to analogues of crab larval-release pheromones. Journal of Crustacean Biology 9, 517524.Google Scholar
De Vries, M.C., Rittschof, D. and Forward, R.B. Jr (1991) Chemical mediation of larval release behaviours in the crab Neopanope sayi. Biological Bulletin. Marine Biological Laboratory, Woods Hole 180, 111.Google Scholar
DeCoursey, P.J. (1979) Egg-hatching rhythms in three species of fiddler crabs. In Naylor, E. and Hartnoll, R.G. (eds) Cyclic phenomena in marine plants and animals: Proceedings of the 13th European Marine Biology Symposium. Oxford: Pergamon Press, pp. 399406.Google Scholar
Derby, C.D. (2000) Learning from spiny lobsters about chemosensory coding of mixtures. Physiology & Behaviour 69, 203209.Google Scholar
Ennis, G.P. (1973) Endogenous rhythmicity associated with larval hatching in the lobster Homarus gammarus. Journal of the Marine Biological Association of the United Kingdom 53, 531538.CrossRefGoogle Scholar
Ennis, G.P. (1975) Observations on hatching and larval release in the lobster Homarus americanus. Journal of the Fisheries Research Board of Canada 32, 22102213.Google Scholar
Fernández, M. and Brante, A. (2003) Brood care in brachyuran crabs: the effect of oxygen provision on reproductive costs. Revista Chilena de Historia Natural 76, 157168.Google Scholar
Fernández, M., Pardo, L.M. and Baeza, J.A. (2002) Patterns of oxygen supply in embryo masses of brachyuran crabs throughout development: the effect of oxygen availability and chemical cues in determining female brooding behaviour. Marine Ecology Progress Series 245, 181190.Google Scholar
Ferrer, R.P. and Zimmer, R.K. (2007) The scent of danger: arginine as an olfactory cue of reduced predation risk. Journal of Experimental Biology 210, 17681775.Google Scholar
Förster, C. and Baeza, J.A. (2001) Active brood care in the anomuran crab Petrolisthes violaceus (Decapoda: Anomura: Porcellanidae): grooming of brooded embryos by the fifth pereiopods. Journal of Crustacean Biology 21, 606615.CrossRefGoogle Scholar
Forward, R.B. Jr (1987) Larval release rhythms of decapod crustaceans: an overview. Bulletin of Marine Science 41, 165176.Google Scholar
Forward, R.B. Jr and Lohmann, K.J. (1983) Control of egg hatching in the crab Rhithropanopeus harrisii (Gould). Biological Bulletin. Marine Biological Laboratory, Woods Hole 165, 154166.Google Scholar
Forward, R.B. Jr, Rittschof, D. and De Vries, M.C. (1987) Peptide pheromones synchronize crustacean egg hatching and larval release. Chemical Senses 12, 491498.CrossRefGoogle Scholar
Forward, R.B. Jr, Lohmann, K. and Cronin, T.W. (1982) Rhythms in larval release by an estuarine crab (Rhithropanopeus harrisii). Biological Bulletin. Marine Biological Laboratory, Woods Hole 163, 287300.Google Scholar
McClary, M. (1997) Chemoreception mediates gregarious settlement of the barnacle Balanus amphitrite amphitrite (Darwin). PhD dissertation. Duke University, USA.Google Scholar
McPhie, D. and Atema, J. (1984) Chemical communication in lobsters: information currents. Biological Bulletin. Marine Biological Laboratory, Woods Hole 167, 510511.Google Scholar
Pettis, R.J., Erickson, B.W., Forward, R.B. Jr and Rittschof, D. (1993) Superpotent synthetic tripeptide mimics of the mud-crab pumping pheromone. International Journal of Peptide and Protein Research 42, 312319.CrossRefGoogle ScholarPubMed
Rittschof, D. (1993) Body odors and neutral-basic peptide mimics: a review of responses by marine organisms. American Zoologist 33, 487493.Google Scholar
Rittschof, D. and Cohen, J.H. (2004) Crustacean peptide and peptide-like pheromones and kairomones. Peptides 25, 15031516.Google Scholar
Rittschof, D., Forward, R.B. Jr and Mott, D.D. (1985) Larval release in the crab Rhithropanopeus harrisii (Gould): chemical cues from hatching eggs. Chemical Senses 10, 567577.Google Scholar
Rittschof, D., Forward, R.B. Jr, Simons, D.A., Reddy, P.A. and Erickson, B.W. (1989) Peptide analogs of the mud crab pumping pheromone: structure–function studies. Chemical Senses 14, 137148.Google Scholar
Saigusa, M. (1982) Larval release rhythm coinciding with solar day and tidal cycles in the terrestrial crab Sesarma—harmony with the semilunar timing and its adaptive significance. Biological Bulletin. Marine Biological Laboratory, Woods Hole 162, 371386.Google Scholar
Saigusa, M. (1992) Control of hatching in an estuarine terrestrial crab I. Hatching of embryos detached from the female and emergence of mature larvae. Biological Bulletin. Marine Biological Laboratory, Woods Hole 183, 401408.CrossRefGoogle Scholar
Saigusa, M. (1994) A substance inducing the loss of premature embryos from ovigerous crabs. Biological Bulletin. Marine Biological Laboratory, Woods Hole 186, 8189.Google Scholar
Saigusa, M. and Hidaka, T. (1978) Semilunar rhythm in the zoea-release activity of the land crabs Sesarma. Oecologia 37, 163176.Google Scholar
Schiffmann, E. (1982) Leukocyte chemotaxis. Annual Review of Physiology 44, 553568.Google Scholar
Schmidt, M. and Ache, B.W. (1996) Processing of antennular input in the brain of the spiny lobster, Panulirus argus. Journal of Comparative Physiology A—Sensory Neural and Behavioural Physiology 178, 605628.Google Scholar
Sokal, R. and Rohlf, F. (1995) Biometry. New York: W.H. Freeman & Co.Google Scholar
Tankersley, R., Bullock, T., Forward, R.B. Jr and Rittschof, D. (2002) Larval release behaviours in the blue crab Callinectes sapidus: role of chemical cues. Journal of Experimental Marine Biology and Ecology 273, 114.Google Scholar
Wachowiak, M., Diebel, C.E. and Ache, B.W. (1996) Functional organization of olfactory processing in the accessory lobe of the spiny lobster. Journal of Comparative Physiology A—Sensory Neural and Behavioural Physiology 178, 211226.Google Scholar
Wilson, J.E.H. (1985) Sublethal effects of diflubenzuron (dimilin) on the reproduction and photobehaviour of the grass shrimp Palaemonetes pugio Holthuis (Caridea, Palaemonidae). PhD dissertation. Duke University, USA.Google Scholar
Ziegler, T. and Forward, R.B. Jr (2007a) Control of larval release in the Caribbean spiny lobster, Panulirus argus: role of chemical cues. Marine Biology 152, 589597.Google Scholar
Ziegler, T.A. and Forward, R.B. Jr (2007b) Larval release behaviours in the Caribbean spiny lobster, Panulirus argus: role of peptide pheromones. Journal of Chemical Ecology 33, 17951805.Google Scholar
Zimmer, R.K. and Ferrer, R.P. (2007) Neuroecology, chemical defense, and the keystone species concept. Biological Bulletin. Marine Biological Laboratory, Woods Hole 213, 208225.CrossRefGoogle ScholarPubMed