Symposium: Ontogenetic Strategies of Invertebrates in Aquatic Environments.

SPEAKERS and LIST of TALKS (as of Sept. 19)

Guy Charmantier (Université Montpellier II, France), Donna L. Wolcott (North Carolina State University):
"Introductory note".

Nora B. Terwilliger, M. Ryan (University of Oregon, Charleston):
"Ontogeny of crustacean respiratory proteins".

John I. Spicer (University of Plymouth, U.K.):
"Development of cardiac function in crustaceans: patterns, processes and implications".

Guy Charmantier (Université Montpellier II, France):
"Ontogeny of osmoregulation in crustaceans: the embryonic phase".

Ernest S. Chang (Bodega Marine Laboratory, University of California):
"Hormones in the lives of crustaceans: an overview".

Robert N. Jinks (Franklin and Marshall College, Pennsylvania), T. L. Markley, G. M. Perovitch, C. Epifanio, T. W. Cronin:
"Ontogeny of vision in marine crustaceans".

Steven C. Hand (Louisiana State University):
"Induction of quiescence and diapause during life cycles of aquatic invertebrates: mechanisms and implications".

Klaus Anger (Biologische Anstalt Helgoland, Germany):
"Life-history adaptations of decapod crustaceans to non-marine conditions".

Richard B. Forward (Nicholas School of the Environment, Marine Lab, Duke University, North Carolina): "Ontogenetic changes in crustacean larval behavior: contributions to transport and settlement".

Craig M. Young (Harbor Branch Oceanographic Institution, Florida), Elsa Vazquez, Ib Svane:
"Early life-history strategies of sessile invertebrates in stratified fjords and coastal lagoons".

Michael G. Hadfield (Kewalo Marine Laboratory, University of Hawaii):
"Metamorphic competence as a major adaptive convergence in marine invertebrate larvae".

Donna L. Wolcott (North Carolina State University): Panel moderator
Discussion and summary session.


7:50 Introduction (G. Charmantier and D. L. Wolcott)
8:00 . N. B. Terwilliger, M. Ryan
8:40 . J. I. Spicer
9:20 . G. Charmantier
10:00/10:20 . Break
10:20 . E. S. Chang
11:00 . R. N. Jinks, T. L. Markley, G. M. Perovitch, C. Epifanio, T. W. Cronin
11:40 . S. C. Hand
12:20/13:40 . Break
13:40 . K. Anger
14:20 . R. B. Forward
15:00/15:20 . Break
15:20 . C. M. Young, E. Vazquez, I. Svane
16:00 . M. G. Hadfield
16:40/17:20 . Discussion and summary session (D. L. Wolcott)

ABSTRACTS (as of Sept. 19)

Overview: Guy Charmantier (Université Montpellier II, France), Donna L. Wolcott (North Carolina State University): "Introductory note" .
Aquatic organisms are subjected to multiple environmental factors wielding a selection pressure upon them. As natural selection acts on all developmental stages, the successful establishment of a species in a given habitat depends on the ability of each of its developmental stages to accommodate these external conditions and their variations. Species may show congruence in behavioral and physiological strategies that are constrained by the rigors of the aquatic environment, especially during development. The evolutionary consequences are important, and have generated increasing interest. The symposium, which brings together physiologists and ecologists, aims at a better understanding of ontogenetic strategies in aquatic environments, and their evolutionary significance. The symposium will successively focus, largely in crustaceans, on the ontogeny of gas exchange (N.B. Terwilliger and M. Ryan), cardiac function (J.I. Spicer), osmoregulation (G. Charmantier), the appearance of hormonal coordinations (E.S. Chang), on vision (R.N. Jinks et al .), on induction of quiescence and diapause (S.C. Hand), and on transition to non-marine conditions (K. Anger). Behavioral and ecological aspects of transport, settlement (R.B. Forward, C.M. Young et al .), and metamorphic competence (M.G. Hadfield) in several invertebrate phyla will also be addressed. D.L. Wolcott will act as panel moderator.

Nora B. Terwilliger, M. Ryan (University of Oregon, Charleston):
"Ontogeny of crustacean respiratory proteins".
The respiratory proteins hemocyanin (Hc) and hemoglobin (Hb) share the function of oxygen transport, but the proteins, their active sites and the metal ions that bind the oxygen are totally different. Either Hc or Hb, but not both, is expressed in the hemolymph of many arthropod crustaceans. Hb is present in Branchiopoda, Ostracoda, Copepoda, rhizocephalan Cirripedia and one suborder of amphipodan Malacostraca while Hc has been described in Malacostraca. Recent work by several laboratories has provided new information on the gene structure, site of synthesis and expression of branchiopod Hbs and suggests they are excellent model organisms for studies of hypoxia sensors and oxygen response elements during development and adult stages. Studies on Hc ontogeny have shown functional changes in Nephrops and Homarus Hcs. The focus in our laboratory on the ontogeny of Hc in the Dungeness crab has demonstrated that both structure and function of Hc change from megalopa to adult crab. The Hc of an oceanic megalopa contains 4 subunits. A 5th subunit appears about the time of metamorphosis to 1st juvenile instar, and expression of a 6th subunit begins four or five molts later. The timing of onset of adult Hc can be altered by food availability and/or temperature. Experiments testing the potential role of magnesium concentration on regulation of Hc ontogeny point to non-specific stress as an additional factor in the timing of the development shift from juvenile to adult Hc. We have identified a Hc-like protein in nauplii and juvenile Artemia using mono- and polyclonal antibodies. This may indicate simultaneous expression of both Hb and Hc gene families in the same organism.

John I. Spicer (University of Plymouth, UK)
"Development of cardiac function in crustaceans: patterns, processes and implications"
While our knowledge of cardiovascular function in adult crustaceans is reasonable, our understanding of how that function comes into being during ontogeny is still, quite literally, embryonic. In this presentation I will briefly outline the different patterns of the onset and development of cardiac function in different crustacean groups. Thereafter our current understanding of the mechanisms underpinning the development of cardiac regulation will be presented together with an assessment of future research priorities. Finally the wider importance of studying the development of cardiac function will be explored. This includes using the crustacean heart as a model for studying the ontogeny of physiological regulation and linking life history characteristics to heart rate variability during early development.

Guy Charmantier (Université Montpellier II, France)
“Ontogeny of osmoregulation in crustaceans : The embryonic phase.”
Three patterns of ontogeny of postembryonic osmoregulation have been recognized in crustaceans : (1) osmoregulation varies little with development stage and the adults are weak regulators or osmoconformers; (2) the adult type of efficient osmoregulation is established in the first postembryonic stage; (3) metamorphosis marks the appearance of the adult type of osmoregulation, generally along with the occurrence of ion-transporting cells and Na-K ATPase in diverse organs. This review will concentrate on the ontogeny of osmoregulation in embryos, particularly in species belonging to type 2 : they are euryhaline and so are their hatchlings. Embryos are osmotically protected against variations in environmental salinity levels, either by closed incubating pouches (in some cladocerans and isopods), semi-closed pouches (where osmolality is at least partially controlled by the diverted female urine, in some amphipods), or more generally by egg membranes (in species whose eggs are directly exposed to the ambient medium). In some species, temporary (e.g. dorsal organs in amphipods) or definitive (e.g. gills in crayfish) osmoregulatory organs, where ionocytes are located, develop in embryos and the activity of Na-K ATPase increases concomitantly. The ability to osmoregulate is thus acquired during the embryonic development, resulting in osmoregulating hatchlings, which is a necessary and key adaptation for species spending their entire life-cycle at low (particularly in fresh water), high or variable salinity.

Ernest S. Chang (Bodega Marine Laboratory, University of California)
“Hormones in the lives of crustaceans: An overview.”
Decapod crustaceans have been a particularly interesting and rewarding group of animals for the study of comparative endocrinology. Most of the published studies, however, have dealt with the hormones of the adult stage; relatively few studies have addressed the hormones of the embryonic and larval stages. The most widely studied hormones during crustacean ontogeny are the arthropod molting hormones--the ecdysteroids. Following a brief survey of crustacean endocrinology, I will present a selected review of what is known about ecdysteroids in the various crustacean life stages. The ecdysteroids are multifunctional and are involved in a number of life processes (growth, regeneration, and reproduction). I will also discuss aspects of the terpenoid hormone methyl farnesoate and the crustacean hyperglycemic hormone neuropeptide family during ontogeny.

Robert N. Jinks, T.L. Markley (Franklin and Marshall College, Pennsylvania), G.M. Perovitch, C. Epifanio (University of Delaware), T.W. Cronin (University of Maryland)
“Ontogeny of vision in marine crustaceans.”
Eyes of most adult crustaceans are specialized for image formation and frequently for color vision or polarization vision as well; but those of larvae probably have more basic functions. In contrast, eyes of adult crustaceans found at hydrothermal vents lack image-forming optics and are specialized for the monochromatic detection of dim light. We studied the ontogeny of vision in the Pacific vent crab Bythograea thermydron . Adults of this species live at a depth of about 2500 m, but the larvae are probably pelagic, and the megalopae swim actively to settle at the vents. Eyes of four developmental stages (megalopa, juvenile 1 and 3, and adult), were examined with electron microscopy (TEM) and/or microspectrophotometry. B. thermydron megalopal visual pigment absorbs maximally at ~479 nm, and is thus well-suited for detection of downwelling light. Juvenile 1 (post-megalopa) eyes have rhabdoms with orthogonal microvilli like those of surface crabs with imaging eyes (e.g. Hemigrapsus ), but lack a dioptric apparatus. Rhabdoms of juvenile 3 retinas are hypertrophied relative to those in retinas of either juvenile 1 or size-matched Hemigrapsus. Absorbance of adult visual pigment is red-shifted (peak ~489 nm) compared to that of the megalopae; however, TEM examination found no neural retina in adult eyes. Megalopal and juvenile 1 retinas may be adapted to a pelagic/mesopelagic existence, while juvenile 3 and adult retinas are better suited to detect the dim, long-wavelength light emitted by hydrothermal vents. Remodeling of structure and function at metamorphosis is probably a common feature in crustacean visual development.

Steven C. Hand (Louisiana State University)
“Induction of Quiescence and Diapause During Life Cycles of Aquatic Invertebrates: Mechanisms and Implications.”
With one exception, all major animal phyla contain species that display dormancy at certain points in their life cycles, a feature that affords tolerance to harsh or ephemeral habitats. Diapause is an obligate, developmentally-programmed form of dormancy that precedes the onset of environmental insult. Under conditions that normally promote activity and development, calorimetric/respirometric studies have revealed that major metabolic depressions accompany entry into diapause in aquatic invertebrates like sponge gemmules and brine shrimp embryos. This depression occurs rather slowly over a period of several days. Release from diapause can be promoted by various environmental cues and artificial chemical factors. Metabolism increases 500-fold or more. In contrast to diapause, quiescence is a type of dormancy directly induced by an environmental stress like oxygen deprivation. Data from many aquatic species show that survivorship under anoxia is proportional to the degree of metabolic depression. There is a suite of molecular mechanisms underlying these metabolic and developmental patterns. In the nucleo-cytoplasmic and mitochondrial compartments, gene expression is severely depressed at transcriptional and translational levels, as assessed by nuclear run-on and cell-free translation assays. Direct measurements of protein and mRNA half-lives indicate that macromolecular turnover is greatly reduced. Stress proteins of low molecular mass undergo intracellular translocation to the nucleus. These and other molecular changes associated with natural states that border on suspended animation provide clues as to how other cells might be placed into stasis. (NSF Grant IBN-9723746)

Klaus Anger (Biologische Anstalt Helgoland, Germany)
“Life-history adaptations of decapod crustaceans to non-marine conditions”
The evolutionary transition from the sea to freshwater or terrestrial environments requires special life-history adaptations, which are exemplified with grapsid crabs from the island of Jamaica and palaemonid shrimps from the Amazon region. As a phylogenetic convergence, limnic and terrestrial species show a reduced planktonic larval phase, large egg size, low fecundity, and larval tolerance of low osmotic pressure. Similar adaptations have been observed in transitional (brackish and semiterrestrial) coastal habitats which are characterized by short duration, great variability in physico-chemical conditions, and unpredictable food production. Crabs that reproduce in temporal supratidal shore or mangrove pools show an ontogenetically early appearance of osmoregulatory functions, allowing for larval tolerance of variable salinities. Low or unreliable plankton production selects for an enhanced energy storage in the eggs, decreasing the nutritional vulnerability during larval development. Intraspecific variability in the endotrophic potential (facultative lecithotrophy) of the early larval stages, as well as cannibalism and benthic behavior in late stages suggest a bet-hedging strategy. It allows resource exploitation and maximum larval growth when food is temporarily available, but also some survival when food is absent. Flexibility is found also in the reproduction of freshwater shrimps: populations living in eutrophic lakes and rivers or in leaf litter of oligotrophic streams produce eggs throughout the year, while those in seasonally inundated forests reproduce only during the period of increasing water, maximizing the dispersal and access of larvae to new food sources. Bet-hedging strategies in temporary habitats may play a significant role in the evolutionary transition from the sea to non-marine environments.

Richard B. Forward (Nicholas School of the Environment, Marine Lab, Duke University, North Carolina)
“Ontogenetic changes in crustacean larval behavior: contributions to transport and settlement.”
Larval development of many estuarine decapod crustaceans occurs in coastal/oceanic areas. Thus, larvae are transported seaward from estuaries for development and then shoreward and up-estuaries to nursery areas as post-larvae. This paper will focus on selective tidal stream transport (STST) as the mechanism for horizontal movement in estuarine areas. The behavior underlying STST varies with species and is based on either a biological rhythm in activity or behavioral responses to environmental factors associated with tides. Transport of post-larvae terminates upon settlement and metamorphosis in nursery areas. Both positive (e.g. odor from conspecifics and aquatic vegetation) and negative (e.g. ammonium, hypoxia, predator odor) cues for habitat selection and metamorphosis will be considered.

Craig M. Young (Harbor Branch Oceanographic Institution, Florida), Elsa Vazquez (University of Vigo, Spain), Ib Svane (Flinders University of South Australia)
"Early life-history strategies of sessile invertebrates in stratified fjords and coastal lagoons."
The larvae of sessile marine animals, unlike those of many crustaceans, are faced with the difficult challenge of selecting a habitat that will be appropriate for the entire adult life. Although the ultimate habitat choice occurs at the time of settlement, many processes occurring in the water column prior to settlement help determine whether larvae will have the opportunity to make an appropriate settlement choice. Most ascidians are stenohaline marine animals that penetrate only short distances into water of low or variable salinity. In coastal lagoons of Florida, the diversity of ascidians is high near inlets but decreases rapidly as a function of distance from the inlets. In laboratory pycnoclines, larvae of colonial ascidians become inactive when swimming into brackish surface layers. This causes them to sink toward the bottom where salinity is highest. Metamorphosis is delayed or inhibited in brackish water and those species that are best able to metamorphose at low salinities are also able to penetrate into brackish portions of the lagoons. In Gullmarsfjorden, Sweden, most ascidians are found below the permanent pycnocline and few are ever found in brackish "Baltic" water that lies above the pycnocline. Experimental transplants and lab incubation experiments indicate that adults of Ascidiella spp. tolerate brackish water but that low salinity inactivates or kills larvae and inhibits metamorphosis. A dense band of Ascidiella aspersa found just below the pycnocline is explained by flotation of embryos and by larval responses to the pycnocline layer. The occasional appearance of Ascidiella scabra in very shallow water appears to result from short-term mixing events which coincide with times when larvae are present in the water column. In both the fjord and lagoon system, the tolerances and responses of ascidians to low salinity change with ontogeny, and processes occurring in the embryonic and larval phases help position the adults in appropriate salinity regimes.

Michael G. Hadfield (Kewalo Marine Laboratory, University of Hawaii)
“Metamorphic competence as a major adaptive convergence in marine invertebrate larvae”
Larvae from diverse and unrelated marine-invertebrate phyla are able to rapidly respond to environmental cues to settlement and to undergo very rapid metamorphogenesis because they share the developmental trait of metamorphic competence. This developmental state, characteristic of larvae as diverse as those of cnidarian planulae, molluscan veligers, and barnacle cyprids, is one in which nearly all requisite juvenile characters are present in the larva prior to settlement. Thus metamorphosis, in response to more or less specific environmental cues (inducers), is mainly restricted to loss of larva-specific organs and physiological processes. Competent larvae of two “model marine invertebrates” studied in the author’s laboratory, the serpulid polychaete Hydroides elegans and the nudibranch Phestilla sibogae , complete metamorphosis in about 12 and 20 hrs, respectively. Furthermore, little or no de novo gene action appears to be required for the settlement and metamorphosis response in these species. Contrasting greatly with the slow, hormonally regulated metamorphic transitions of vertebrates and insects, rapid metamorphosis in marine invertebrate larvae is conjectured to have arisen in diverse phylogenetic clades as a response to common environmental pressures that favor extremely fast transition from larval locomotory and feeding modes, adapted to life in the plankton, to a different set of such modes, adapted to life on the sea bottom.

Donna L. Wolcott (North Carolina State University) Panel moderator
Discussion and summary session .