Ian R. Jenkinson Agency for Consultation and Research in Oceanography, Hydrosphere Biorheology Laboratory, 19320 La Roche Canillac, France [email protected]

Deformation, adhesion, recognition and genes in the hydrosphere: What are the relative importances of D'Arcy-Thompsonian and Darwinian structuring? Types of deformation Deformation in the hydrosphere (fresh, sea, and other natural waters) occurs: 1. in 3D, as in the bulk phase of the water; 2. in 2D, as in water-air films, and films around bubbles. Resistance to deformation in liquids and solids.. When a material is deformed non-compressively, the resistance to deformation can be decomposed into two components: viscous (in which the energy expended in deformation is lost to heat) and elastic (in which the energy is stored and is recovered on relaxation of the deformation). Most of us learn at high-school that viscosity is characteristic of Newtonian liquids (like pure alcohol, water or glycerol), and elasticity of Hookean solids (almost like rubber or iron). The characteristic resistance forces are termed respectively the viscous and elastic moduli. In a Newtonian liquid the viscous modulus is proportional to the deformation rate and there is no elasticity, but in a Hookean solid the elastic modulus is proportional to deformation (period). Resistance to deformation in polymer-containing materials. It is well-known (by rheologists, but alas not by limnologists or oceanographers) that the deformation of polymer-rich materials, including foods pharmaceutical products, sewage, etc., is a mixture of viscous and elastic, and its characterisation is termed its rheological properties. In polymeric materials, the viscous component is not generally proportional to shear rate, the relationship depending on the molecular structure of the polymer. As well, in heterogeneous (granular or lumpy) materials the rheological properties depend on the length scale of measurement or of the process concerned (Coussot, 2005; Jenkinson & Wyatt, 2008). Rheological properties of the hydrosphere. Fresh and sea water (the hydrosphere), both in the water column and associated with sediments or organisms, is a solution of dissolved organic matter (DOM), a colloid of colloidal organic matter, and a suspension of particulate organic matter (POM) including marine organic aggregates, transparent exopolymers (TEP).and bits of organisms. Many of the cells of planktonic bacteria (Fig. 1), algae (Fig. 2) and metazoa are covered with a glycocalyx.. Like in metazoa, it is becoming increasingly clear (Wootton et al 2008) that protozoans also use lectins (carbohydrate-protein complexes) in cell-cell and cell-other recognition. The rheological properties of seawater are not trivial, as the combined viscous-elastic modulus has been found in a Phaeocystis blooms to be nearly 10-100 times higher than that of pure seawater (at a length-scale of 0.5 mm and a deformation rate of 0.002 s- 1 in the apparatus shown in Fig 3 (Jenkinson 1993). The moduli inside mucus aggregates like those in Fig 4. are likely to be orders of magnitude higher again. In investigations of the rheological properties of benthic algal “fluff”, and algal cultures in relation to ventilation and respiration by fish, it was difficult to assess the length and deformation scales involved. We (Jenkinson et al, 2007a,b) invented ichthyoviscometers using the gill ways of a dead fish to physically model those of a live one. Cell-cell and cell-other adhesive forces, although important in ecological interaction, are still rarely measured directly. They constitute a branch of small-scale or micro-rheology. Biologically increased viscosity may also act on the stability and thickness of thin layers associated with pycnoclines (GEOHAB 2008), and the mechanical properties of polymers may interfere with copepod grazing (Malej & Harris 1993). D'Arcy-Thompsonian vs. Darwinian structuring The proposals of Wyatt & Ribera d'Alcalà (2006) are, I suggest required reading They erect largely testable hypotheses for how different types of exopolymeric substances (EPS) may, under genetic control, structure the pelagic world. This is termed “planktonic engineering”. My aim is not to duplicate them here but use them as a basis for supplementary suggestions.

The forms of macromolecules, organelles, cells, organs, organisms and the structures they make (such as diatom frustules, mollusc shells, phytoplankton or zooplankton colonies, or even the lobate and filamentous forms of a Noctiluca bloom seen from the air, or a coral reef) are taxon-specific. They result from gene expression, itself the object of Darwinian (Darwin, 1861) selection. Yet, as elegantly shown by D'Arcy Thompson (1917), many of these structures bear a close resemblance to abiological structures formed by spontaneous ordering, and Thompson proposed that organisms use abiological ordering, called “order for free” by Kauffman (1993) thereby economising the genetic effort needed (Gould, 2002). The ocean, like freshwater bodies, is not an organism, but like organisms, it has genes that control, guide or influence its structures and forms, to make them different from what would be present in the sole presence of spontaneous abiological ordering. DOM, TEP, Organic aggregates and flux Most of this material is formed by gene expression, but Wells & Goldberg (1993) showed spontaneous aggregation of DOM into colloids. Kiørboe et al (1994) applied coagulation theory to explain formation of flocs by diatom cells in a shear field. An important parameter is the “stickiness” of the diatoms, expressed as the likelihood (0 to 1) of sticking, but this has not been expressed as physical forces. While break-up of sinking or rising aggregates is clearly important to their vertical speed and organic flux. But perhaps because it was perceived that biological interference was important in break-up, work on aggregate mechanical strength (Alldredge et al, 1990; Jenkinson et al, 1991) unfortunately has not continued. Surface-film, 2D Rheology Much DOM and TEP and many organic aggregates are sticky or surface-active, and in some cases perhaps associated with buoyancy (Riebesell, 1992; Mari 2008), accumulate at the surface and become electrically bound to it (Žutić et al., 1981; Ćosović et al., 2005). This organic surface film is visible in calm weather when it forms slicks, which have marked surface rigidity at a time scale of 100 min, as shown in Fig. 6. These films influence air-water exchange of gas, water vapour and organic matter itself under both calm and rough conditions. The 2D compression-dilation (CD) surface-film rheology is current measured using a Langmuir trough and a Wilhelmy plate (Fig. 7), often with simultaneous electrochemical measurements that help reveal the molecular changes during CD. Basin scale effects and biogeochemistry The Ocean, like other water bodies is a bioreactor. Although not an organism, its components, particularly pelagic structures and processes involving extracellular organic matter, are partly determined by interaction between D'Arcy-Thompsonian spontaneous order formation and Darwinian selection of genes, particularly those genes involved in the fixation, degradation and transformation of this organic matter By acting partly through the rheological properties and density of this organic matter, genes influence many biogeochemical processes. Need to bring rheological expertise into research teams In order to properly appreciate the physical effects of DOM, TEP and organic aggregates on the diffusion, dispersion and small-scale circulation in the hydrosphere, as well as effects on grazing, and both gas and nutrient exchange, rheological expertise should be sort by oceanographic research teams. At an international rheology conference (Jenkinson, 2008), a group of rheologists formed, interested to take part in discussions or research with oceanographers. I can share this small list with anyone interested Summary and conclusions The rheological properties of the hydrosphere are contributed by water+salt and by the exopolymeric matter it contains. These properties, along, notably, with density, determine organic flux, diffusion, exchange and dispersion of most substances and properties. The rheological properties of the organic matter interactively determine its own flocculation and break-up through selective adhesion and aggregate strength. Polymer rheological properties affect food-web interactions, and basin-scale biogeochemical processes. Because hardly any collaboration takes place between pelagic oceanographers and rheologists, little realisation exists in either field of the need for rheological investigation of the hydrosphere. A small group of rheologists interested in working with ocean scientists recently formed, however, and this interested must be exploited.

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Fig. 1. Marine-aggregate bacteria stick together via a glycocalyx never touching directly. Cells of multicellular animals, algae and plants are similar (Biddanda, 1986)

Fig. 2. Light micrograph of Chattonella antiqua (Raphidophyceae), illustrating glycocalyx on the cell surface. Scale bar = 5 μm; gc: glycocalyx. (Photo: T. Honjo)

Fig.4. Algal polymers during exceptional mucus event due to diatom polymers in Adriatic Sea (Flander-Putrle & Malej, 2008)

Fig 6. Photograph of surface wake pattern, 100 min after the passage of a Navy ship (Peltzer et al. 1992)

Fig 3. Classical shearing rheometer (Contraves LS 30) Couette geometry (Jenkinson 1986; 1993; Jenkinson & Biddanda 1995)

Fig. 5. Mark 3 ichthyoviscometer (not to scale) (Jenkinson et al. 2007b)

Fig 7. Surface visco-elasticity and surface potential measured with a Langmuir trough (oscillating surface “wiper”, Wilhelmy plate and differential electrometer) (Dragčević & Pravdić 1981)

References: Alldredge, A., Granata, T., Gotschalk, C. & Dickey, T. (1990) The physical strength of marine snow and its implications for particle disaggregation in the ocean. Limnol. Oceanogr., 35, 1415-1428 Biddanda, B.A. (1986) Structure and function of marine microbial aggregates. Oceanologica Acta 9:209-211. Ćosović, B. (2005) Surface-Active Properties of the Sea Surface Microlayer and Consequences for Pollution in the Mediterranean Sea In Saliot, A. (ed.) The Mediterranean Sea Springer, Berlin, 269-296 Coussot, P.(2005) Rheometry of Pastes, Suspensions, and Granular Materials. Wiley, Hoboken, NJ Darwin, C.R. (1861). On the Origin of Species by Natural Selection, John Murray, London. Dragćević, D. & Pravdić, V. (1981). Properties of the seawater-air interface. 2. Rates of surface film formation under steady state oscillations. Limnol. Oceanogr., 26, 492-499. Flander-Putrle, V. & Malej, A. (2008) The evolution and phytoplankton composition of mucilaginous aggregates in the northern Adriatic sea Harmful Algae, 7, 752-771 GEOHAB Global Ecology and Oceanography of Harmful Algal Blooms (2008) GEOHAB Core Research Project: HABs in Stratified Systems, P. Gentien, B. Reguera, H. Yamazaki, I. Fernand, E. Berdalet, R. Raine (Eds.). IOC and SCOR, Paris, France, and Newark, Delaware, USA, 59 pp. Gould, S. J. (2002) The Structure of Evolutionary Theory Harvard Univ Press, Cambridge, Mass. Jenkinson, I.R. (1986) Oceanographic implications of non-Newtonian properties found in phytoplankton cultures. Nature, 323, 435-437 Jenkinson, I. R. (1993) Bulk-phase viscoelastic properties of seawater. Oceanologica Acta, 16, 317-334 Jenkinson, I. R. (2008) Ocean Rheology and Plankton Biology In Co, A., Leal, L G., Colby, R.H. & Giacomin, A.J. (eds.) The XVth International Congress on Rheology, Am. Inst.Phys., 636-638. Jenkinson, I., Biddanda, B., Turley, C., Abreu, P., Riebesell, U. & Smetacek, V. (1991) Rheological properties of marine organic aggregates: importance for vertical flux, turbulence and microzones. Oceanologia Acta, Sp. Vol. No. 11, 101-107 Jenkinson, I.R. & Biddanda,B.A. (1995) Bulk-phase viscoelastic properties of seawater: relationship with plankton components J. Plankton Res., 17, 2251-2274 th Jenkinson, I.R. & Wyatt, T. (2008).Rheological properties of exopolymeric secretions in HABs may be functions of length scales. In Moestrup, Ø. et al. (eds), Proc. 12 int. Conf. Harmful Algae, ISSHA and IOC of UNESCO, Copenhagen, pp. 126-128. Jenkinson, I. R.; Claireaux, G. & Gentien, P. (2007a) Biorheological properties of intertidal organic fluff on mud flats and its modification of gill ventilation in buried sole Solea solea Mar Biol, 150, 471-485 Jenkinson, I.R., Shikata, T. & Honjo, T.(2007b) Modified ichthyoviscometer shows high viscosity in Chattonella culture Harmful Algae News, No. 35, 1, 3-5 Kauffman, S.A. (1993). The Origins of Order, Oxford Univ Press, New York. Kiørboe, T., Lundsgaard, C., Olesen, M. & Hansen, J.L S.(1994) Aggregation and sedimentation processes during a spring phytoplankton bloom: A field experiment to test coagulation theory J mar Res, 52, 297-323 Malej, A. & Harris, R. (1993) Inhibition of copepod grazing by diatom exudates: a factor in the development of mucus aggregates? Mar. Ecol. Prog. Ser., 96, 33-42 Peltzer, R.D., Griffin, O.M., Barger, W.R. & Kaiser, J.A.C. (1992) High-resolution measurement of surface-active film redistribution in ship wakes .J. geophys. Res., 97(C4), 5231-5252. Mari, X. (2008) Does ocean acidification induce an upward flux of marine aggregates? Biogeosciences, 5, 1023-1031 Riebesell, U. (1992) The formation of large marine snow and its sustained residence in surface waters Limnol. Oceanogr, 37, 63-76 Thompson, D'Arcy W. (1917) On Growth and Form Cambridge Univ Press, England Wells, M. & Goldberg, E. (1993). Colloid aggregation in seawater. Mar. Chem, 41, 353-358 Wootton, E., Zubkov, M. V., Jones, D.H., Jones, R. H., Martel, C M., Thornton, C. A. & Roberts, E. C.(2008) Biochemical prey recognition by planktonic protozoa Environm Microbiol, 9, 216-212 Wyatt, T. & Ribera d'Alcalà, M. (2006) Dissolved organic matter and planktonic engineering CIESM Workshop Monographs, No. 28, 13-23 Žutić, V., Ćosović, B, Marćenko, E. & Bihari, N. (1981) Surfactant production by marine phytoplankton. Mar Chem. 10, 505-520