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JEB Classics 3431 A CLASSIC far ahead of his time he was in applying JEB Classics is an occasional HYDRODYNAMIC hydrodynamic theory to understand larval column, featuring historic responses to water flow in the boundary publications from The Journal of ANALYSIS OF LARVAL layer just above the surface of the Experimental Biology. These SETTLEMENT attachment site. articles, written by modern experts in the field, discuss each classic In his 1955 paper, Crisp addressed a now paper’s impact on the field of central issue in marine larval ecology, biology and their own work. A namely if and how microscopic larvae can PDF of the original paper actively select final settlement sites on accompanies each article, and shores and seabeds exposed to water flows can be found on the journal’s more than 100ϫ faster than larval website as supplemental data. swimming speeds. In a series of elegant experiments, Crisp explored how barnacle larvae (cyprids) respond to water flow at the surface of a potential attachment site, and how flow speed may prevent swimming cyprids from making an initial attachment to a surface. In well-defined flow regimes Crisp first determined the swimming capability of different species of cyprids. He then tested the ability of free- swimming cyprids to attach to surfaces exposed to different flow speeds. His pioneering approach was to focus on the local flow speed at the scale of the settling larva (ca. 0.5 mm), rather than the free- stream flow speed away from the seabed. s Per R. Jonsson writes about D. J. Crisp’s By applying hydrodynamic theory Crisp 1955 publication on the behaviour of was perhaps the first to explicitly point out barnacle cyprids in relation to water the significance of the velocity gradient of movement over a surface. water (the boundary layer), which is c always present close to any surface, to Dennis Crisp began his academic education aquatic organisms. In his experiments Crisp i in Cambridge, where he studied natural used glass tubes of different diameters to sciences with a broad coverage in physics, create a series of velocity gradients at the chemistry and biology (see biography by attachment surface. Crisp knew that the Fogg and Southward, 1992). His first velocity distribution in laminar water flow s scientific achievements dealt with physico- through pipes is easily determined and he chemical mechanisms involved in protein could relate larval attachment probability to surface affinity. This background, the local flow speed acting on the larvae when making contact with the solid s combined with a deep interest in zoology, led to a post at a commercial testing station surface. He showed that local flow speeds –1 for studies of corrosion and fouling on of a few cm s stimulated cyprid man-made surfaces in the marine attachment, which then declined sharply when he increased flow speeds to a environment. Here, Crisp began his life- long research to understand the factors 10–20 cm s–1. Crisp also found that controlling the settlement behaviour of the cyprids, once attached, could use their l larval stage of marine organisms. During antennae to walk along the substrate the golden era of British marine larval surface at even higher local flow speeds biology in the 1950s, he rapidly became than 10–20 cm s–1. Crisp explained the one of the most influential scientists in the cyprid’s ability to remain attached by C development of larval ecology. During his showing that the hydrodynamic drag acting career he published several comprehensive on the cyprid body was considerably less studies detailing the responses of marine than the predicted adhesion force generated larvae to environmental factors in their by its antennae against the substratum. He quest for a suitable site to metamorphose concluded that of all the processes involved into the sedentary, adult life stage (e.g. in larval settlement, initial adhesion is the B Crisp, 1955, 1974; Crisp and Barnes, 1954; most sensitive to flow speed. Crisp and Meadows, 1963). Crisp’s classic paper on the effect of water flow on the Crisp also found an interesting E settlement of barnacle larvae, published in correspondence between the swimming The Journal of Experimental Biology in velocity of cyprids and the local flow speed 1955, continues to have a positive citation that resulted in maximum attachment. He J trend 50 years after its publication. The proposed a mechanism of site selection growing citation frequency attests to how based on flow, where cyprids approaching THE JOURNAL OF EXPERIMENTAL BIOLOGY JEB Classics 3432 the surface swim against the current hydrodynamic forces took time to diffuse References (rheotaxis) and attach when local flow into the marine biological community. Abelson, A. and Denny, M. (1997). Settlement speed coincides with their swimming However, Crisp’s paper clearly foreshadows of marine organisms in flow. Ann. Rev. Ecol. speed. However, he offered no explanation the successful application of hydrodynamics Syst. 28, 317-339. as to how the suspended cyprid could in aquatic ecology that developed in the Butman, C. A. (1987). Larval settlement of obtain some frame of reference against 1980s. I can only guess that research soft-sediment invertebrates: the spatial scales which it could exercise a rheotactic following in the footsteps of Crisp’s paper of pattern explained by active habitat selection response. This mechanism of larval choice was stimulated by his quantitative use of and the emerging rôle of hydrodynamical still remains to be tested. With the hydrodynamic theory (e.g. Butman, 1987; processes. Oceanogr. Mar. Biol. Ann. Rev. 25, inclusion of a boundary layer Crisp partly Eckman et al., 1990; Mullineaux and 113-165. resolved the debate of how larvae could Butman, 1991). It is clear that the issue of Crimaldi, J. P., Thompson, J. K., Rosman, J. H., Lowe, R. J. and Koseff, J. R. (2002). settle in water currents where the free- flow effects on larval settlement first raised Hydrodynamics of larval settlement: the stream flow greatly exceeds larval in Crisp’s 1955 paper is now at the core of influence of turbulent stress events at potential swimming speeds. A limitation in Crisp’s larval ecology research. recruitment sites. Limnol. Oceanogr. 47, 1137- analysis is that all his experimental 1151. boundary layers were laminar, whereas Personally, I am deeply impressed with the Crisp, D. J. (1955). The behaviour of barnacle most marine attachment sites likely scholarship evident in Crisp’s work, how cyprids in relation to water movement over a experience turbulent water flow. Crisp was ahead of his time he was with this surface. J. Exp. Biol. 32, 569-590. well aware of this simplification, but at that publication, and the skill he showed in his Crisp, D. J. (1974). Factors influencing the time empirical information about time- experiments on live larvae. In a recent settlement of marine invertebrate larvae. In Chemoreception in marine organisms (ed. P. T. dependent turbulent boundary-layer flow paper on the settlement of barnacle cyprids Grant and A. M. Mackie), pp. 177-265. London: was not available. Recent work shows that in different flow environments (Jonsson et Academic Press. the prediction of settling probability is al., 2004) we found that the data on critical Crisp, D. J. and Barnes, H. (1954). The much more complex in turbulent boundary flow speeds for attachment in cyprids orientation and distribution of barnacles at layers (Abelson and Denny, 1997; presented in Crisp’s paper are still the best settlement with particular reference to surface Crimaldi, 2002). available, despite the tremendous contour. J. Anim. Ecol. 23, 142-162. developments in high-speed video Crisp, D. J. and Meadows, P. S. (1963). The The key innovation in Crisp’s paper was the recording and flow measurement chemical basis of gregariousness in cirripedes. rigorous inclusion of hydrodynamic theory techniques in recent years. In his classic Proc. R. Soc. B 156, 500-520. Eckman, J. E., Savidge, W. B. and Gross, T. F. to gain an understanding of the flow 1955 paper, Dennis Crisp reported a very (1990). Relationship between duration of cyprid conditions and forces acting on the small fine piece of research with both theoretical attachment and drag forces associated with scale of larvae. Possibly because he was and empirical qualities. Few scientific detachment of Balanus amphitrite cyprids. Mar. trained in physics and chemistry Crisp had reports stand the test of time so well. Biol. 107, 111-118. the theoretical ability to cross the traditional Fogg, G. E. and Southward, A. J. (1992). discipline boundaries and combine A PDF file of the original paper can be accessed online: Dennis John Crisp. Biogr. Mem. 38, 111-129. hydrodynamic theory and experimental http://jeb.biologists.org/cgi/content/full/208/18/3431/DC1 Jonsson, P. R., Berntsson, K. M. and Larsson, A. I. (2004). Linking larval supply to ecology. It is probably fair to say that the 10.1242/jeb.01824 power of applying hydrodynamic analysis to recruitment: flow-mediated control of initial adhesion of barnacle larvae. Ecology 85, 2850- better understand larval settlement was not Per R. Jonsson 2859. fully recognized at the time of publication. Tjärnö Marine Biological Laboratory Mullineaux, L. S. and Butman, C. A. (1991). The biological audience was apparently not Marine Ecology Initial contact, exploration and attachment of prepared for the physical message. The Göteborg University barnacle (Balanus amphitrite) cyprids settling in significance of the boundary layer and [email protected] flow. Mar. Biol. 110, 93-103. THE JOURNAL OF EXPERIMENTAL BIOLOGY.