Larval Release Rhythms and Larval Behavior of Palinurid Lobsters: A Comparative Study (original) (raw)
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LOBSTERS: A COMPARATIVE STUDY by
2007
This dissertation investigated larval release and larval behavior of the Caribbean spiny lobster Panulirus argus and the spotted spiny lobster P. guttatus. These species were examined under laboratory conditions to determine the phase relationship between larval release and natural environmental cycles. P. argus displayed a nocturnal tidal rhythm, while P. guttatus displayed a circadian rhythm in larval release. P. argus releases larvae near the time of nocturnal high slack water, while P. guttatus released larvae near the time of sunrise. The role of 'pumping pheromones' in controlling larval release behaviors was tested by measuring the pumping response of ovigerous P. argus to (1) hatch water, (2) homogenized-embryo water, (3) embryo-conditioned water, and (4) water containing homogenized-egg cases. Lobsters with late-stage embryos displayed increased pleopod pumping with increased concentration of hatch water. Water individually conditioned with homogenized late-stage embryos, intact late-stage embryos, and homogenized eggcases induced pumping activity in females with late-stage embryos, indicating the presence of a chemical cue. I quantified pumping responses upon exposure to synthetic peptides to determine if they mimicked pheromones that induce larval release behaviors. Pumping behavior was evoked by oligopeptides with a basic amino acid at the carboxy-terminus, v preceded by several neutral amino acids. Carboxyl-terminal arginine peptides serve as pheromone mimics. I investigated whether these peptides originate from the action of trypsin-like enzymes by conducting a bioassay measuring pumping activity of ovigerous P. argus subjected to increasing concentrations of trypsin, trypsin inhibitor, and a combination of the two. Pumping activity increased with increasing concentrations of trypsin and trypsin inhibitor, while behaviors ceased when ovigerous females were subjected to a complex of the two. Pheromones are generated by trypsin-like enzymes assisting in the degradation of the egg membranes at the time of hatching. Vertical swimming behaviors of stage-I phyllosoma larvae of P. argus and P. guttatus were observed under laboratory conditions. P. argus larvae displayed a pattern of twilight vertical migration, while P. guttatus larvae displayed nocturnal diel vertical migration (DVM). Rhythms persisted for 5-6 cycles under constant conditions, indicating that an endogenous rhythm in activity plays a proximate role in DVM for both species. vi Dedication This work is dedicated to the memories of my father, Charles A. Ziegler II, my sister Christine J. Ziegler, my aunt Susan F. Holl, and my best friends Loretta D. Abel
Control of larval release in the Caribbean spiny lobster, Panulirus argus: role of chemical cues
Marine Biology, 2007
The current model for larval release in subtidal crustaceans suggests that hatching time is controlled by the embryos, which release a pheromone that stimulates the parent female to undergo behaviors that synchronize larval release. Alternatively, hatching could be controlled by the females. Ovigerous spiny lobsters Panulirus argus (Latreille) exhibit stereotypic behaviors during larval release, including rapid abdominal extensions and pleopod-pumping activity. Ovigerous P. argus were collected from coral reefs in the Florida Keys, USA during the summers of 2005 and 2006. Pleopod-pumping activity was quantiWed to determine if a female's pumping activity correlates with the developmental state of the embryos. The role of pheromones released by developing and hatching embryos in controlling pumping behaviors was tested by measuring the pumping response of ovigerous lobsters to (1) hatch water, (2) homogenized embryo water, (3) embryo-conditioned water (unhatched late-stage embryos soaked for 20 h), and (4) water containing homogenized post-hatch embryo cases. Bioassays were conducted under constant conditions (dim-red light) in the laboratory at random times during the day to control for any possible rhythm in pumping activity. Spontaneous pleopod-pumping activity increased signiWcantly with increasing embryo development. Upon exposure to hatch water, ovigerous lobsters with late-stage embryos displayed increased pleopod pumping with increased treatment concentration. Water individually conditioned with homogenized late-stage embryos, intact late-stage embryos, and homogenized post-hatch embryo cases all induced larval release behaviors in females with late-stage embryos. Ovigerous females with early-stage embryos did not respond to water conditioned with homogenized early-or late-stage embryos. These results suggest that active substances are released by embryos at the time of hatching and induce the stereotypical pumping behaviors of the female that synchronizes larval release. The results support the model that larval release in subtidal crustaceans is controlled by pheromones released from hatching embryos.
Journal of Experimental Marine Biology and Ecology, 2010
Blue crabs Callinectes sapidus, like most decapods, synchronously hatch eggs and release larvae over a very short time period. Synchrony is achieved though vigorous abdominal pumping in response to pheromones from hatching eggs. We hypothesized that these or related pheromones stimulate vertical swimming associated with larval release and ebb-tide swimming during the last few days before egg hatching. We used abdominal pumping and swimming assays to investigate the roles of pheromones. We tested responses of crabs to egg extract containing pheromones, trypsin (an enzyme that generates peptide pheromones), and bradykinin (a peptide pheromone mimic). We delivered test substances directly into the egg mass via capillary tubing. In response to egg extract, ovigerous crabs increased abdominal pumping and vertical swimming, showing native pheromones evoke both behaviors. Delivery of trypsin and bradykinin caused increased pumping but not vertical swimming. These results suggest that pheromones generated from eggs stimulate vertical swimming during ebb-tide transport, but that peptides that induce abdominal pumping are not sufficient to cause swimming. We hypothesize that swimming is stimulated by a blend of molecules that includes these peptide pheromones.
Chemical Mediation of Larval Release Behaviors in the Crab Neopanope sayi
The Biological Bulletin, 1991
Control of egg hatching was investigated in ovigerous females of the crab Neopanope sayi. Larval release is a brief event, generally lasting less than 15 min, during which females perform stereotypic behaviors involving vigorous abdomen pumping. Substances released by hatching eggs (pumping factors) of N. sayi, Rhithropanopeus harrisii, and Uca pugilator, but not Sesarma cinereum, evoked these stereotypic behaviors (pumping response) in ovigerous N. sayi. Spontaneous pumping and responsiveness to pumping factors varied with the age of the embryos. These results indicate that the eggs release pheromones around the time of hatching, which supports the general model for egg-hatching control described for R. harrisii (Forward and Lohmann, 1983). The chemistry of N. sayi pumping factors was investigated, and the pumping response was used as a bioassay in this study. Pumping factors adsorbed to Amberlite XAD-7 resin and could be eluted from it with methanol. Size fractionation by cascade pressure dialysis showed that the active molecules were < 1000 daltons. Acid hydrolysis followed by reverse-phase HPLC amino acid analysis showed that the biologically active fraction contained peptides. Cysteine, glycine, methionine, and isoleucine were the four most common amino acids in these peptides. The responsiveness of N. sayi to hatch water from R. harrisii, the general similarity of adsorptive characteristics of hatch waters from the two species toward XAD-7 resin, and the amino acid compositional analysis suggest that the pumping factors from both species are similar. This supports the hypothesis that N. sayi pumping factors are also small peptides, as was suggested for those of R. harrisii (Rittschof et al., 1985, 1989).
Larval release behaviors in the blue crab Callinectes sapidus: role of chemical cues
Journal of Experimental Marine Biology and Ecology, 2002
Egg hatching by brachyuran crabs is often precisely timed relative to environmental cycles and may be controlled by the female, the developing embryos, or both. The current conceptual model for larval release in subtidal brachyuran crabs is that the exact time of release is controlled by the developing embryos. At the time of hatching, the eggs release pheromones that induce stereotypic larval release behaviors in ovigerous females consisting of rapid abdominal pumping. This behavior breaks open the eggs and results in synchronized hatching. To test this model, we examined the role of pheromone substances released by developing and hatching eggs in initiating this pumping behavior in ovigerous blue crabs Callinectes sapidus. Pumping behavior was used as a bioassay to determine if pumping activity changes with the developmental state of the eggs and to test the response of ovigerous crabs to (1) substances released by hatching eggs (hatch water), (2) substances present in homogenized eggs containing early-and late-stage embryos (homogenized egg water), and (3) substances released by developing eggs containing early-and late-stage embryos (egg conditioned water). Pumping activity associated with egg maintenance increased with embryo development. Pumping activity increased with increasing concentration of hatch water and the threshold concentrations for females possessing early-and late-stage eggs were similar. Water containing homogenized eggs also evoked larval release behaviors and response thresholds were the same for females exposed to early-and late-stage egg treatments. Egg conditioned water prepared from eggs containing late-stage embryos was more potent than water prepared from eggs with earlystage embryos. Collectively, these results support the model that larval release in C. sapidus is controlled by pheromones released from hatching eggs and indicate that (1) the responsiveness of ovigerous C. sapidus to the pheromones is relatively independent of the stage of embryo development, (2) homogenates of both early-and late-stage eggs contain similar pheromone
Journal of Chemical Ecology, 1990
Studies of crab egg hatching and larval release behavior in the crab, Rhithropanopeus harrisii, generated a model describing the process. In the model, carboxyl terminal arginine peptides serve as pheromones that synchronize larval release. In response to the peptides, the female performs stereotypic larval release behavior and casts larvae into the water column. The peptides originate from trypsin-like enzymatic activity as part of the egghatching process. Hatching can be simulated experimentally by incubating ovigerous crabs in either bovine or porcine trypsin. The female performs the larval release behavior. Eggs detach from the female, and immobile larvae hatch prematurely. Preincubation of trypsin with trypsin inhibitors eliminates these effects. Approximately nanomolar concentrations of five different polypeptide trypsin inhibitors evoke the female's larval release behavior. Because both peptides and trypsin inhibitors evoke larval release behavior and because trypsin inhibitors bind to both the peptide receptor and the enzyme with high affinity, the receptor binding site and trypsin catalytic site must be very similar. A relationship between the binding site of a peptide receptor and the catalytic site of trypsin is postulated. The difference may be substitution by a basic amino acid for the catalytic site serine. Molecular graphics modeling indicates that all necessary conditions for receptor binding can be met by substitution with lysine for the active site serine in the trypsin catalytic site. This substitution eliminates catalytic activity, maintains the binding affinity for trypsin inhibitors, and increases binding strength for peptides.
The Biological Bulletin, 2010
Phyllosoma larvae of the spiny lobster Panulirus argus undergo diel vertical migration (DVM), in which they are at depth during the day and nearer the surface at night. This study determined the visual spectral sensitivity of Stage I larvae and investigated whether light plays a proximate role in DVM as an exogenous cue and as an entrainment cue for an endogenous rhythm in vertical migration. Under constant conditions, larvae have a circadian rhythm (24.5-h period) in vertical swimming that resulted in a twilight DVM pattern. The behavioral response spectrum and electroretinogram recording indicated two photoreceptor spectral classes with maxima at 360 and 486 nm. When stimulated in an apparatus that simulated the underwater angular light distribution, dark-adapted larvae showed only positive phototaxis, with a threshold intensity of 1.8 ϫ 10 13 photons m-2 s-1 (3.0 ϫ 10-5 moles photons m-2 s-1). They have an avoidance response to predator shadows in which they descend upon sudden decreases in light intensity of more than 69%. When stimulated with relative rates of decrease in light intensity as occur at sunset they ascended, whereas they descended upon relative rates of light intensity increase as occur at sunrise. Thus, the DVM pattern is controlled by both an endogenous circadian rhythm in swimming and behavioral responses to light at sunrise and sunset.
Crustacean peptide and peptide-like pheromones and kairomones
Peptides, 2004
Crustacean peptide pheromones, kairomones, and substituted amino sugar kairomones are reviewed from a historical perspective. These crustacean information molecules are secondary functions of structural polymers. They are partial hydrolysis products, generated usually by the action of trypsin-like enzymes on proteins, and glycosidase enzymes on glycoproteins and proteoglycans. Structure-function studies based upon synthetic mimics of peptide information molecules show neutral amino acids with a basic carboxyl terminal are active in modifying physiological and or behavioral responses. Behaviorally active substituted amino sugar mimics are disaccharide hydrolysis products of heparin and chondroitin sulfate. Similar molecules are also used as information molecules by a variety of other marine organisms indicating they are a common biological theme.
Peptide-mediated behaviors in marine organisms Evidence for a common theme
Journal of Chemical Ecology, 1990
Biology has many common themes such as DNA, RNA, the other biopolymers, and their building blocks. Chemical communication systems have similar common themes. An example is the common usage of amino acids, sugars, and nucleotides as food cues. It is likely that communication systems began with the evolution of specific meanings for preexisting molecules. One class of molecules used in specific communication is peptides. These peptides are generated as part of the body odor of organisms in aquatic environments and can act at a distance or by contact. Evidence is given for a common type of peptide receptor system. Four peptide-mediated behaviors, three in diverse crustacean groups and one in a mollusc, are discussed. The behaviors are of major survival importance, are cued by nanomolar concentrations of peptides generated by serine proteases, and the basic carboxy terminal amino acid is required. The behaviors include attraction to new shells, attraction to living prey, release of larvae, and induction of larval settlement behavior. Studies with pure di-and tripeptides show the same molecules evoke larval release behavior, shell attraction responses, and larval settlement behavior. The pure compounds are effective at nanomolar or lower concentrations. Similar peptides function as specific cues in vertebrates in response to wounding. Thus, peptide communication using serine protease-generated peptides appears to be a common theme,
Pheromones inhibit the hatching of diapausing Anostraca (Crustacea: Branchiopoda
Hatching of resting eggs of Streptocephalus torvicornis (Waga, 1942) and Branchipus schaefferi Fischer, 1834, two sympatric fairy shrimps, was tested using medium in which these two species and Chirocephalus diaphanus (Prévost, 1803) had been raised. The medium of adults inhibited the hatching of conspecific nauplii, even when diluted by 50% using distilled water. Streptocephalus torvicornis resting eggs hatch in the medium of C. diaphanus but not in the medium of B. schaefferi. Resting eggs of B. schaefferi hatched in low numbers in S. torvicornis medium, and in high numbers in that of C. diaphanus.