SEPTEMBER 2010 R O U S S E A U E T A L . 2107 On Turbulence Production by Swimming Marine Organisms in the Open Ocean and Coastal Waters SHANI ROUSSEAU,* ERIC KUNZE,RICHARD DEWEY,KEVIN BARTLETT, AND JOHN DOWER SEOS, University of Victoria, Victoria, British Columbia, Canada (Manuscript received 15 December 2009, in final form 24 April 2010) ABSTRACT Microstructure and acoustic profile time series were collected near Ocean Station P in the eastern subarctic North Pacific and in Saanich Inlet at the south end of Vancouver Island, British Columbia, Canada, to ex- amine production of turbulent dissipation by swimming marine organisms. At Ocean Station P, although a number of zooplankton species are large enough to generate turbulence with Reynolds numbers Re . 1000, biomass densities are typically less than 103 individuals per cubic meter (,0.01% by volume), and turbulent kinetic energy dissipation rates « were better correlated with 16-m vertical shear than acoustic backscatter layers. In Saanich Inlet, where krill densities are up to 104 individuals per cubic meter (0.1% by volume), no dramatic elevation of dissipation rates « was associated with dusk and dawn vertical migrations of the acoustic backscatter layer. Dissipation rates are a factor of 2 higher [h«i 5 1.4 3 1028 Wkg21, corresponding to buoyancy Re 5 h«i/(nN2) ; 140] in acoustic backscatter layers than in acoustically quiet waters, regardless of whether they are vertically migrating. The O(1 m) thick turbulence patches have vertical wavenumber spectra for microscale shear commensurate with the Nasmyth model turbulence spectrum. However, the turbulence bursts of O(1025 Wkg21) proposed to occur in such dense swarms appear to be rare. Thus far, intense turbulent bursts have been found infrequently, even in very dense aggregations O(104 individuals per cubic meter) characteristic of coastal and high-latitude environs. Based on sampling to date, this corresponds to a frequency of occurrence of less than 4%, suggesting that turbulence production by the marine biosphere is not efficient. 1. Introduction quantify the possible impact on ocean turbulence and mixing. Turbulence production in the stratified ocean interior Energetic arguments suggest that significant turbulent is largely attributed to breaking internal gravity waves dissipation rates might be generated by aggregations of generated by (i) atmospheric forcing at the surface and swimming marine organisms. Based on the Reynolds (ii) tidal flow over topography (Munk and Wunsch 1998). numbers of individual organisms, Huntley and Zhou While it has long been known that swimming marine (2004) predicted turbulent kinetic energy dissipation organisms produce a turbulent wake (Wiese and Ebina « ; 25 21 1995; Yen 2000; Yen et al. 2003; Catton et al. 2008), the rates O(10 Wkg ) for organisms ranging from research focus has been on the energetic and detection 0.5-cm-long zooplankton to cetaceans, a value compara- consequences for these organisms (e.g., Enders et al. ble to that driven by storms in surface waters. Globally, 2003; Pitchford et al. 2003). Little has been done to Dewar et al. (2006) estimated that up to 1 TW might be available from swimming marine organisms, assuming 30 Gt of biomass [equivalent to ;O(0.1%) by volume if distributed over the upper 100 m], comparable to the * Current affiliation: Que´bec-Oce´an, De´partement de Biologie, Universite´ Laval, Quebec City, Quebec, Canada. 2 TW needed for abyssal mixing, 0.8 TW of deep-ocean tidal dissipation (Egbert and Ray 2001), and 1 TW of deep-ocean wind forcing (Wunsch and Ferrari 2004); Corresponding author address: Eric Kunze, SEOS, University for comparison, global human power consumption of Victoria, P.O. Box 3055, STN CSC, Victoria BC V8W 3P6, Canada. was 15 TW in 2008. Munk (1966) came up with simi- E-mail: [email protected] lar numbers for the energy available for biologically DOI: 10.1175/2010JPO4415.1 Ó 2010 American Meteorological Society Unauthenticated | Downloaded 09/28/21 11:28 AM UTC 2108 JOURNAL OF PHYSICAL OCEANOGRAPHY VOLUME 40 generated turbulence by assuming that 20% of bi- to 105 are high enough that a high turbulent mixing effi- ological consumption was used for swimming. Because ciency (g ; 0.2) would be expected. Moreover, they were the bulk of the ocean’s biomass is found in the upper few accompanied by strong temperature-gradient micro- hundred meters and his primary interest was in abyssal structure (though the complicated thermohaline vari- mixing, he did not pursue this thread further. Bi- ability in Saanich Inlet precludes quantifying a reliable ologically generated turbulence is unlikely to play a sig- mixing efficiency) and density overturns on the length nificant role in the meridional thermohaline circulation scales expected for the observed dissipation rates [LO 5 because of biomass’s intensification toward the surface («/N3)1/2]. and coastal zones. Even more anecdotal evidence comes from a single If 1 TW is distributed over the upper 100 m, it im- profile collected in a dense aggregation of krill being fed plies average turbulent kinetic energy dissipation rates upon by a pod of humpback whales in Soquel Canyon, h«i ; 5 3 1028 Wkg21 [corresponding to a buoyancy California, during August 2008, which revealed dissipa- Reynolds number h«i/(nN2) 5 500]. This is well within tion rates of 1026 Wkg21, the highest during the cruise, the detection limit of conventional microstructure pro- exceeding dissipation rates found in the near-bottom filers (Dewey et al. 1987). stratified turbulent layer (Kunze et al. 2010) by an order Much of any turbulence generated by swimming ma- of magnitude. In contrast, Rippeth et al. (2007) found no rine organisms is likely to occur in the surface boundary elevated turbulence associated with diel migration of the layer, which is already well mixed by atmospheric forc- acoustic backscatter layer in 13 dawn and dusk time series ing. However, many schooling species exhibit diel ver- from the western continental shelf of the British Isles. tical migration through stratified waters of the upper Another issue is how often biologically generated tur- pycnocline. During daylight, they evade predation by bulence does any mixing. Measurements by Gregg and resting in the dark below 100-m depth, surfacing at Horne (2009) in Monterey Bay fish aggregations ex- nightfall to feed (Forward 1988). Biologically generated hibited high turbulent kinetic energy dissipation rates, turbulence from such diel vertical migratory species could as previously reported by Farmer et al. (1987), but with potentially mediate transport of nutrients and dissolved (i) microscale shear spectra depleted at low wavenumber gases between the surface mixed layer and underlying and (ii) very weak temperature-gradient microstructure 2 2 stratified waters where mixing processes are not well xT and hence low mixing efficiency g 5 N xT /(Tz«) # understood (Johnston and Rudnick 2009). This could 0.0022, where xT is the turbulent temperature variance contribute to providing nutrients to maintain biological dissipation rate. On the other hand, Lorke and Probst productivity in the often nutrient-depleted euphotic zone. (2010) inferred mixing efficiencies g 5 0.2 associated with Assuming an upper-ocean buoyancy frequency N 5 turbulence generated by shoals of perch in Lake Con- 1022 rad s21 and an upper-bound mixing efficiency g ; 0.2 stance but reported dissipation rates « two orders of (Osborn 1980; Oakey 1982), h«i ; 5 3 1028 Wkg21 cor- magnitude smaller than predicted by either the bio- responds to diapycnal eddy diffusivities K 5 gh«i/N2 ; mechanical arguments of Huntley and Zhou (2004) or 1024 m2 s21. Purely physical mesoscale (McGillicuddy metabolic arguments. Gregg and Horne (2009) suggested and Robinson 1997; McGillicuddy et al. 1998, 1999) and that the fish aggregations responsible for their high tur- submesoscale (Mahatavan and Tandon 2006) mecha- bulent dissipation rates created shear too close to the nisms have also been proposed for transporting nutri- Kolmogorov scale (n3/«)1/4 ; O(1 cm) (Tennekes and ents into the euphotic zone (Klein and Lapeyre 2009). Lumley 1972), which was then viscously squelched rather Kunze et al. (2006) reported observational evidence than generating broadband turbulence and efficient mix- for biologically generated turbulence in Saanich Inlet, ing, an argument consistent with grid-generated turbu- British Columbia (BC), Canada, a sheltered fjord at the lence experiments (Itsweire et al. 1986). In contrast, south end of Vancouver Island. During the 28 April 2005 shear-driven turbulence [reduced shear Vz 2 2N . 0(Sun dusk upward migration of an acoustic backscatter layer et al. 1998) or, equivalently, gradient Richardson number composed of the krill species Euphausia pacifica with Ri , 0.25] is generated at the largest (Ozmidov) scales up to 104 individuals per cubic meter (0.1% by volume; («/N3)1/2 ; O(1 m), allowing turbulence to overcome De Robertis et al. 2003), they observed a coincident 10– stratification and cascade energy down to Kolmogorov 15-min burst of turbulence with dissipation rates of scales through nonlinear interactions, provided LO LK, 1025 to 1024 Wkg21 between 50- and 100-m depths, before being viscously damped. consistent with the predictions of Huntley and Zhou Although capable of generating turbulence, individ- (2004). These measurements had microstructure shear ual zooplankton and small fish may not be able to mix spectra that fit the Nasmyth (1970) model turbulence efficiently because their lengths are comparable to the spectra. Buoyancy Reynolds numbers Re 5 «/(nN2) 5 104 Kolmogorov length scales. However, the coordinated Unauthenticated | Downloaded 09/28/21 11:28 AM UTC SEPTEMBER 2010 R O U S S E A U E T A L . 2109 movement of a dense aggregation might produce turbu- anywhere from a 1 in 10 to 1 in 1000 chance of sampling lence at the thickness of such aggregations with outer (i) in an aggregation.