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Control of Larval Release in the Caribbean Spiny Lobster, Panulirus Argus: Role of Chemical Cues

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Control of Larval Release in the Caribbean Spiny Lobster, Panulirus Argus: Role of Chemical Cues Mar Biol DOI 10.1007/s00227-007-0712-2 RESEARCH ARTICLE Control of larval release in the Caribbean spiny lobster, Panulirus argus: role of chemical cues Tracy A. Ziegler · Richard B. Forward Jr Received: 14 February 2007 / Accepted: 17 April 2007 © Springer-Verlag 2007 Abstract The current model for larval release in subtidal with homogenized late-stage embryos, intact late-stage crustaceans suggests that hatching time is controlled by the embryos, and homogenized post-hatch embryo cases all embryos, which release a pheromone that stimulates the induced larval release behaviors in females with late-stage parent female to undergo behaviors that synchronize larval embryos. Ovigerous females with early-stage embryos release. Alternatively, hatching could be controlled by the did not respond to water conditioned with homogenized females. Ovigerous spiny lobsters Panulirus argus (Latr- early- or late-stage embryos. These results suggest that eille) exhibit stereotypic behaviors during larval release, active substances are released by embryos at the time of including rapid abdominal extensions and pleopod-pump- hatching and induce the stereotypical pumping behaviors ing activity. Ovigerous P. argus were collected from coral of the female that synchronizes larval release. The results reefs in the Florida Keys, USA during the summers of 2005 support the model that larval release in subtidal crusta- and 2006. Pleopod-pumping activity was quantiWed to ceans is controlled by pheromones released from hatching determine if a female’s pumping activity correlates with the embryos. developmental state of the embryos. The role of phero- mones released by developing and hatching embryos in controlling pumping behaviors was tested by measuring the Introduction pumping response of ovigerous lobsters to (1) hatch water, (2) homogenized embryo water, (3) embryo-conditioned Larval release in most decapod crustaceans is under endog- water (unhatched late-stage embryos soaked for 20 h), and enous control and is synchronized with environmental (4) water containing homogenized post-hatch embryo cases. cycles, such as light:dark, tidal, or lunar cycles (see For- Bioassays were conducted under constant conditions ward Jr 1987; Morgan 1995 for reviews). Larval release (dim-red light) in the laboratory at random times during the is a brief event that is associated with speciWc behaviors of day to control for any possible rhythm in pumping activity. the female (DeCoursey 1979; Forward Jr et al. 1982; De Spontaneous pleopod-pumping activity increased signiW- Vries 1990; Tankersley et al. 2002). In brachyuran crabs, cantly with increasing embryo development. Upon expo- embryos typically hatch all at once over a short time inter- sure to hatch water, ovigerous lobsters with late-stage val as the female prods the egg mass with her walking legs embryos displayed increased pleopod pumping with increased and vigorously pumps her abdomen to help break open the treatment concentration. Water individually conditioned cases containing the embryo within (Forward Jr et al. 1982; Christy 1986; De Vries and Forward Jr 1989). In contrast, in anomuran crabs and lobsters, larvae are released in more Communicated by J.P. Grassle. than one short burst at the time of consecutive tidal phases or nights (Ennis 1973; Branford 1978; Ziegler and Forward T. A. Ziegler (&) · R. B. Forward Jr Jr 2005, 2006). A female lobster will Xex and extend her Duke University Marine Laboratory, X Nicholas School of the Environment and Earth Sciences, abdomen and strongly utter her pleopods back and forth 135 Duke Marine Lab Road, Beaufort, NC 28516, USA during the hatching event. Thus, the temporal control of lar- e-mail: [email protected] val release in decapods appears to vary with species. 123 Mar Biol The time of embryo hatching may be controlled by the (4) substances present in homogenized membranes from behavior of the female, by the developing embryos releas- post-hatch embryo cases. ing a chemical that breaks open embryo cases (membranes that hold and protect the embryo during development), or by some combination of the two. Control of larval release Materials and methods has been examined in the subtidal crabs Rhithropanopeus harrisii (Forward Jr et al. 1982, 1987; Forward Jr and Loh- Collection and maintenance of spiny lobsters mann 1983; Rittschof et al. 1985, 1989), Neopanope sayi (De Vries et al. 1991), and Callinectes sapidus (Tankersley Ovigerous spiny lobsters P. argus (Latreille) were collected et al. 2002). These studies have led to the development of a by hand using SCUBA from June to August 2005 and model for larval release for brachyuran crabs (Forward Jr May to August 2006 at coral reefs near the Keys Marine et al. 1987; De Vries et al. 1991; Tankersley et al. 2002), in Laboratory in the Florida Keys, USA (24°49.567N, which the developing embryos control the exact time of 80°48.884W). Lobsters were maintained in individual glass hatching, whereas the female controls the synchrony of lar- aquaria containing t75 l of continuously aerated seawater val release. Near the time of hatching, the female begins to (salinity of 35–36; 27°C) Wltered to remove particles exhibit larval release behaviors because she is responding >5 m. The size range of ovigerous females used in this to substances released from hatching embryos, termed study was from 64.3 to 92.1 mm carapace length. The water ‘pumping pheromones’. As more embryos hatch, the con- in the aquaria was changed daily at random times. A 14 h centration of the pheromone increases, thereby stimulating light:10 h dark cycle simulated ambient conditions at the the female to initiate more and more vigorous abdominal time of collection. pumping. This pumping activity helps to physically disrupt the embryo case. More pheromone leads to more pumping, Terminology which leads to more breaking of embryonic cases, and this positive feedback system results in the synchronous release A fertilized egg is deWned here as an ‘embryo’. Embryos of larvae. are attached to the maternal ovigerous hairs and are encap- The timing of larval release for the Caribbean spiny lob- sulated in protective membranes, which we refer to as the ster, Panulirus argus, is also precisely timed. Larval release ‘embryo case’. ‘Egg mass’ is deWned as the entire brood of occurs at the time of slack water after nocturnal Xood tides embryos attached to the ovigerous hairs on the pleopods on (T. A. Ziegler, unpublished data). Ovigerous spiny lobsters the abdomen of the female. display stereotypical larval release behaviors similar to A scheme for staging embryo development was con- brachyuran crabs. The female lobster rises onto her walking structed by observing the complete developmental sequence legs, probes her egg mass with the tips of her walking legs of the embryos from oviposition to hatching (Table 1). Ovi- and rapidly Xexes and extends her abdomen while actively gerous females with early-stage embryos were held in the beating the pleopods. During larval release, this vigorous laboratory at constant temperature (27°C) and photoperiod ‘pleopod pumping’ behavior acts to synchronize embryo (14 h light:10 h dark cycle). The developmental stages of hatching. Homarid lobsters are also known to pump their the embryos for P. argus were determined by microscopic pleopods during the hatching process as a physical mecha- analysis to catalog the ontogeny of the diVerent stages nism to release larvae (Ennis 1973, 1975; Branford 1978). (Helluy and Beltz 1991). A small set of embryos (t20) was The objective of this study was to investigate whether removed from the surface of the egg mass of females the model for larval release of subtidal brachyuran crabs (n = 24) at daily intervals. Cleavage, yolk content, eyespot can be applied to P. argus. Although homarid lobsters and development, and chromatophore formation were recorded. brachyuran crabs have been studied, palinurid lobsters have The number of days from the appearance of each develop- not been investigated. We designed the following experi- mental stage to hatching was determined. Since environmen- ments to test the hypothesis that spiny lobster embryos con- tal factors can control the speed of embryo development, this tain substances (pheromones) that prompt the ovigerous provided only a general estimate of the time to hatching for females to initiate the movement of the pleopods that each developmental stage. occurs during larval release. The stereotypical larval release behavior (pleopod EVect of embryonic developmental stage pumping) was used as a biological assay to determine if on pleopod-pumping activity ovigerous spiny lobsters respond to (1) pheromone sub- stances released by hatching embryos, (2) substances pres- To determine if pleopod-pumping activity of female lob- ent in homogenates of early- and late-stage embryos, (3) sters changes with the embryonic development stage, the pheromones released from embryos prior to hatching, and spontaneous pumping rate of ovigerous lobsters carrying 123 Mar Biol Table 1 Embryonic develop- Stage Embryo Description Duration of ment: description of embryo mass color stage (days) development in Panulirus argus in the laboratory at 27°C I Bright orange Cell division not evident; yolk granules throughout t 2–3 II Orange Cleavage visible; blastomeres present 2 III Orange Yolk-free, transparent streak at animal pole, near funiculus; 2 clustering of cells into segments; yolk central IV Orange Eyespots crescent-shaped slivers; structure of appendages 2 visible; yolk occupies 66% embryo
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