Responses of Some Marine Plankton Animals to Changes in Hydrostatic Pressure

Knight‐Jones, E. W.; Qasim, S. Z.

doi:10.1038/175941a0

Cited by 69 publications

(50 citation statements)

References 5 publications

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“…The diversity of sensory neurons with cilia-regulating neuropeptides in the Platynereis larva is consistent with the multitude of environmental cues annelid and other ciliated larvae can respond to. These cues include light, pressure, salinity, and temperature, as well as settlement-inducing chemicals (6,17,18,53). Some of these cues were shown to change the distribution of larvae, either by pro- moting upward swimming (e.g., increased pressure) (53) or by inhibiting cilia (e.g., settlement cues) (17).…”

Section: Discussionmentioning

confidence: 99%

Neuropeptides regulate swimming depth of Platynereis larvae

Conzelmann

Offenburger

Asadulina

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

116

180

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Cilia-based locomotion is the major form of locomotion for microscopic planktonic organisms in the ocean. Given their negative buoyancy, these organisms must control ciliary activity to maintain an appropriate depth. The neuronal bases of depth regulation in ciliary swimmers are unknown. To gain insights into depth regulation we studied ciliary locomotor control in the planktonic larva of the marine annelid, Platynereis. We found several neuropeptides expressed in distinct sensory neurons that innervate locomotor cilia. Neuropeptides altered ciliary beat frequency and the rate of calcium-evoked ciliary arrests. These changes influenced larval orientation, vertical swimming, and sinking, resulting in upward or downward shifts in the steady-state vertical distribution of larvae. Our findings indicate that Platynereis larvae have depth-regulating peptidergic neurons that directly translate sensory inputs into locomotor output on effector cilia. We propose that the simple circuitry found in these ciliated larvae represents an ancestral state in nervous system evolution.neural circuit | zooplankton | sensory-motor neuron | FMRFamide-related peptides T wo different types of locomotor systems are present in animals, one muscle based and the other cilia based. The neuronal control of muscle-based motor systems is well understood from studies on terrestrial model organisms. In contrast, our knowledge of the neuronal control of ciliary locomotion is limited, even though cilia-driven locomotion is prominent in the majority of animal phyla (1).Ciliary swimming in open water is widespread among the larval stages of marine invertebrates, including sponges, cnidarians, and many protostomes and deuterostomes (2-5). Freely swimming ciliated larvae often spend days to months as part of the zooplankton (1, 6). The primary axis for ciliated plankton is vertical, and body orientation is maintained either by passive (buoyancy) or active (gravitaxis, phototaxis) mechanisms. When cilia beat, larvae swim upward, and when cilia cease beating, the negatively buoyant larvae sink. During swimming, the thrust exerted on the body is proportional to the beating frequency of cilia (7-9). The alternation of active upward swimming and passive sinking, together with swimming speed and sinking rate, is thought to determine vertical distribution in the water (8). Because several environmental parameters, including water temperature, light intensity, and phytoplankton abundance, change with depth, swimming depth will influence the speed of larval development, the magnitude of UV damage, and the success of larval feeding and settlement. To stay at an appropriate depth, planktonic swimmers must therefore sense environmental cues and regulate ciliary beating.The ciliated larvae of the marine annelid Platynereis dumerilii provide an accessible model for the study of ciliary swimming in marine plankton (10). Platynereis can be cultured in the laboratory, and thousands of synchronously developing larvae can be obtained daily year-round (11). Platynereis ha...

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Section: Discussionmentioning

confidence: 99%

Neuropeptides regulate swimming depth of Platynereis larvae

Conzelmann

Offenburger

Asadulina

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

116

180

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“…Larval depth distributions-Laboratory studies have shown that the phototaxis and pressure response behavior of barnacle larvae changes through the naupliar and cyprid stages (Knight-Jones and Morgan 1966;Lang et al 1979); thus, it is likely that the depth distributions also change. Direct observations of the depth distributions of barnacle larvae in the Monterey Bay region have been made for Chthamalus spp.…”

Section: Methodsmentioning

confidence: 99%

Dispersal of barnacle larvae along the central California coast: A modeling study

Pfeiffer-Herbert

McManus

Raimondi

et al. 2007

Limnology & Oceanography

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To investigate the biological and physical mechanisms affecting larval dispersal, we embedded a model of Balanus glandula larval development and behavior into physical circulation fields of waters along the central California coast. Physical circulation fields were generated by a three-dimensional ocean circulation model with a horizontal resolution of 1.5 km and 20 topography-following layers in the vertical. The ocean circulation model was forced by air-sea fluxes derived from a mesoscale atmospheric model and assimilated temperature and salinity data from the Autonomous Ocean Sampling Network II experiment. An ecosystem model that calculated chlorophyll a (a proxy for larval food concentration) was also coupled to the ocean circulation model. The coupled model of larval development, larval behavior, food concentration, and physical circulation was used to run simulations of larval dispersal. Simulation results predicted a greater return of larvae to the nearshore waters with relaxation circulation patterns than with upwelling. More larvae were supplied to the coast north of Monterey Bay than to the south, and larvae that successfully returned to the nearshore waters generally had limited dispersal distances. These modeling results agree with previous observations of B. glandula population dynamics in central California.Many intertidal marine species have a planktonic larval phase, and populations in the intertidal zone are largely shaped by the supply of these larvae. An understanding of the pathways of larval dispersal would provide many of the answers to questions about how intertidal populations are connected. However, direct observations of larvae dispersing in coastal waters are very sparse, because of the difficulty of making these observations. An alternative to direct observation is to predict the paths of dispersing larvae with model simulations. In this study, we model the dispersal of Balanus glandula larvae and predict dispersal pathways in coastal waters of central California.To model larval dispersal it is first necessary to understand the biology of the larvae. B. glandula is

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“…Increased levels of activity may indicate a pressure-initiated stress response. Elevated swimming activity in response to increased hydrostatic pressure has been observed in crustacean larvae as an example of behavioural homeostasis (Hardy and Bainbridge, 1951;Knight-Jones and Qasim, 1955;Gherardi, 1995). Elevated levels of active movement exhibited by P. varians may represent an escape response to maintain its optimal bathymetric distribution.…”

Section: Temperature and Pressure Effects On Rates Of Oxygen Consumptmentioning

confidence: 99%

Pressure tolerance of the shallow-water caridean shrimp Palaemonetes varians across its thermal tolerance window

Oliphant

Thatje

Brown

et al. 2011

Journal of Experimental Biology

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2002). The potential for depth range extension and colonisation of the deep sea may, therefore, be genuine for some shallow-water species. There is evidence that the echinoid Echinus acutus has extended its bathymetric range, indicating that migrations to the deep sea are still occurring (Tyler and Young, 1998 Accepted 8 December 2010 SUMMARY To date, no published study has assessed the full physiological scope of a marine invertebrate species with respect to both temperature and hydrostatic pressure. In this study, adult specimens of the shallow-water shrimp species Palaemonetes varians were subjected to a temperature/pressure regime from 5 to 30°C and from 0.1 to 30MPa. The rate of oxygen consumption and behaviour in response to varying temperature/pressure combinations were assessed. Rates of oxygen consumption were primarily affected by temperature. Low rates of oxygen consumption were observed at 5 and 10°C across all pressures and were not statistically distinct (P0.639). From 10 to 30°C, the rate of oxygen consumption increased with temperature; this increase was statistically significant (P<0.001). Palaemonetes varians showed an increasing sensitivity to pressure with decreasing temperature; however, shrimp were capable of tolerating hydrostatic pressures found outside their normal bathymetric distribution at all temperatures. 'Loss of equilibrium' (LOE) in ≥50% of individuals was observed at 11MPa at 5°C, 15MPa at 10°C, 20MPa at 20°C and 21MPa at 30°C. From 5 to 20°C, mean levels of LOE decreased with temperature; this was significant (P<0.001). Low mean levels of LOE were observed at 20 and 30°C and were not distinct (P0.985). The physiological capability of P. varians to tolerate a wide range of temperatures and significant hydrostatic pressure is discussed.

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Responses of Some Marine Plankton Animals to Changes in Hydrostatic Pressure

Cited by 69 publications

References 5 publications

Neuropeptides regulate swimming depth of Platynereis larvae

Neuropeptides regulate swimming depth of Platynereis larvae

Dispersal of barnacle larvae along the central California coast: A modeling study

Pressure tolerance of the shallow-water caridean shrimp Palaemonetes varians across its thermal tolerance window

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