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Behaviour in flow: perspectives on the distribution and dispersion of meroplanktonic larvae in the water column1 Anna Metaxas

Abstract: For marine benthic invertebrates with meroplanktonic larvae, the relative importance of hydrodynamics and swimming behaviour in determining larval dispersal in the water column, particularly at small spatial scales, has not been determined. In the field, larval aggregations recorded at physical and biological discontinuities in the water column were attributed to hydrodynamics. Similar aggregations obtained in the absence of flow in the laboratory indicate a potentially significant role of behaviour. At large spatial scales, larval distribution in the plankton is mainly regulated by horizontal advection. However, the ability of larvae to behaviourally regulate their position at scales of micrometres to metres when exposed to turbulent fluid motion in the water column, as evidenced in the benthic boundary layer, is unknown. Evaluation of swimming in turbulent flows in the water column is an intriguing area of research, which involves several constraints. In the field, quantification of behaviour is limited by low success in tracking larvae and lack of appropriate observational tools. In the laboratory, the generation and quantification of flow regimes that are representative of those in the field remains a challenge. An approach that integrates biological and physical measurements within realistic ranges is necessary to advance our understanding of larval dispersal. Résumé : Pour les invertébrés benthiques marins à phase larvaire méroplanctonique, on n’a pas déterminé l’importance relative de l’hydrodynamique et du comportement de nage dans la dispersion des larves dans la colonne d’eau, particulièrement à de petites échelles spatiales. Sur le terrain, les rassemblements de larves observées à des discontinuités physiques et biologiques de la colonne d’eau ont été attribuées à l’hydrodynamique. Des rassemblements similaires obtenus au laboratoire en l’absence de mouvement de l’eau indiquent que le comportement peut jouer un rôle notable. À de grandes échelles spatiales, la distribution des larves dans le plancton est principalement régie par l’advection horizontale. Toutefois, on ne connaît pas l’aptitude des larves à agir par le comportement sur leur position à des échelles allant du micromètre au mètre quand elles sont exposées à des mouvements turbulents dans la colonne d’eau, comme on l’a observé dans la couche limite benthique. L’évaluation de la nage dans des écoulements turbulents dans la colonne d’eau est un domaine de recherche déroutant qui doit tenir compte de diverses contraintes. Sur le terrain, la quantification du comportement est limitée par le faible succès du pistage des larves, et par l’absence d’outils appropriés d’observation. Au laboratoire, la reconstitution et la quantification de régimes d’écoulement représentatifs de ceux du milieu naturel constituent encore un défi. Une approche intégrant les mesures biologiques et physiques dans des plages réalistes nous est nécessaire pour mieux comprendre la dispersion des larves. [Traduit par la Rédaction]

Invited perspectives and article

Introduction For marine benthic invertebrates with meroplanktonic life cycles, the importance of larval supply in determining the spatial distribution of adult populations is well established (Gaines et al. 1985; Minchinton and Scheibling 1991). However, despite a considerable increase in our understanding of Received January 20, 2000. Accepted June 30, 2000. Published on the NRC Research Press web site on November 8, 2000. J15538 A. Metaxas.2 Department of Oceanography, Dalhousie University, Halifax, NS B3H 4J1, Canada, and Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, U.S.A. 1 2

Invited perspective for this 100th Anniversary Issue. Present address: Department of Oceanography, Dalhousie University, Halifax, NS B3H 4J1, Canada (e-mail: [email protected]).

Can. J. Fish. Aquat. Sci. 58: 86–98 (2001)

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the planktonic larval stages during the last two decades (for a review, see McEdward 1995), the relative importance of factors that determine survival and dispersal while larvae are in the plankton remains elusive (Young and Chia 1987; Rumrill 1990; Young 1995). Several studies have measured larval abundance and distribution in the field, but most have examined effects of different physical (e.g., salinity, temperature, pressure) and biological (e.g., diet, predation) factors on larval behaviour, survival, and development in the laboratory. At present, extrapolation of results from laboratory to field settings is constrained by our limited knowledge of appropriate scaling factors and of the relative importance of the dominant flow regimes. The individual roles of hydrodynamics and swimming behaviour in larval displacement in the water column have been studied extensively. In an overview of factors that regulate horizontal dispersal at large spatial scales (1000s to 10 000s of kilometres), Scheltema (1986) concluded that the current regime was of overriding importance. Shanks

DOI: 10.1139/cjfas-58-1-86

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(1995a) reached a similar conclusion in his evaluation of the studies on cross-shelf transport (100s to 1000s of kilometres) of invertebrate larvae. Focusing on much smaller scales (millimetres to metres), Young (1995) provided a comprehensive review of patterns and cues of swimming behaviour. He and others have suggested that swimming can play an important role at these smaller scales, particularly in vertical displacement of larvae. When larvae are released in the water column, they may remain within the water parcel that overlies the adult habitat, or they may be introduced into a different water layer and get advected by currents (e.g., Pedrotti and Fenaux 1992). Larvae that are advected to the open ocean may be returned to adult habitats in distinct pulses within water parcels that are upwelled or associated with internal bores (Shanks and Wright 1987; Pineda 1994). The boundaries of water parcels usually are delineated by physical and (or) biological discontinuities, such as pycnoclines and layers of chlorophyll maxima, and they may occur at fronts with high shear and pronounced turbulence. To remain near or to be returned to the adult habitat, larvae may have to avoid crossing water parcels, and thus may aggregate at these boundaries. These aggregations could result from a behavioural response to the physical or biological features of the boundaries or from the passive accumulation of organisms with a different specific gravity than the surrounding medium. Although meroplanktonic larvae descend to the benthos near the end of their larval existence, the relative importance of hydrodynamics and behaviour in larval supply to the substratum has been studied extensively and is well understood, particularly at small spatial scales (for reviews, see Butman 1987; Snelgrove and Butman 1994). While in the plankton, larvae generally had been considered to behave as passive tracers because most studies examined their horizontal displacement at large spatial scales and in strong flow regimes. Over the past decade, however, recognition of the potential importance of swimming behaviour in larval displacement in the water column has triggered an expanding body of research. At this early stage, I believe that an evaluation of the advances and limitations of the existing evidence can be beneficial in directing ongoing and future research on this topic. I provide a perspective on the relative importance of hydrodynamics (particularly turbulent flow) and swimming behaviour in generating distributions of invertebrate larvae around physical (haloclines, thermoclines, bores, and fronts) and biological (layer of chlorophyll maximum and food patches) features in the water column. This perspective is premised by our extensive knowledge of factors influencing larval supply to the benthos. Specifically, it is well established that in the benthic boundary layer, hydrodynamics are primarily responsible for delivery of competent larvae to appropriate settlement sites (Butman 1987). However, once these larvae enter the logarithmic layer or the viscous sublayer (i.e., within centimetres to millimetres above the substratum), they selectively settle in response to physical, chemical, and biological cues associated with the bottom (Mullineaux and Butman 1991). Selective settlement can be effectuated by an increased ability of the larvae to regulate their position in reduced flow speeds (Butman 1987) or by increased retention resulting from the vertical shear within the viscous sublayer (Jonsson

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et al. 1991). Similar interactions between hydrodynamics and behaviour may be operating at boundaries in the water column, but only if larvae can alter their swimming behaviour in response to the biological and physical structure in their environment and regulate their position in the dominant flow regime. It should be noted, however, that different selective constraints probably operate during the “dispersive” planktonic period of larval life than during the “retentive” period of competence and settlement within the benthic boundary layer. While in the plankton, larvae generally are positively buoyant, negatively geotactic, and positively phototactic, which causes them to swim away from the bottom and towards the sea surface to seek food and escape predation. In contrast, competent larvae become negatively buoyant, positively geotactic, and negatively phototactic, which increases their probability of descent to the benthos. Where the information on meroplankton is limited, I invoke evidence from studies on holoplankton and fish larvae to propose mechanisms that may be responsible for observed distributional patterns of invertebrate larvae and warrant further study. This indirect evidence should be viewed with caution because some meroplankton are weaker swimmers than holoplankters and larval fish. (For the interested reader, Dower et al. (1997) provided a comprehensive review on behaviour of fish larvae (particularly feeding) in different flows.) I identify deficiencies in our understanding of processes that generate the observed distributions of invertebrate larvae and provide suggestions for future research, both in laboratory and in field settings. In particular, I argue that studies of biological processes (such as larval swimming or feeding) should incorporate detailed measures of physical processes (such as shear or turbulence) to better understand the mechanisms that generate the observed distributional patterns of larvae in the ocean. Because of a perceived inaccessibility to a relatively simple mathematical explanation, accurate quantification of flow is often avoided by biologists despite its paramount importance in these studies. Therefore, I append a basic mathematical treatment of the quantification of turbulent diffusion, which I consider comprehensible to the interested biologist.

Larval distribution around physical features of the water column Spatial distributional patterns of invertebrate larvae in relation to physical features in the water column, such as haloclines, thermoclines, and fronts, have been observed both in descriptive studies in the field and in experimental studies in the laboratory. In the field, larval aggregations at or immediately above or below haloclines have been recorded for several invertebrate taxa, such as the polychaete Owenia fusiformis (Thiébaut et al. 1992) or an assemblage of bivalve veligers (mainly Mytilus edulis) (Raby et al. 1994). On Georges Bank, Northwest Atlantic, Tremblay and Sinclair (1990a) found that the centre of mass of the distribution of veligers was within or immediately above the pycnocline for the giant scallop Placopecten magellanicus. The magnitude of aggregation was positively related to the strength of stratification (Tremblay and Sinclair 1990a), but a minimum stratification may be required for aggregation to occur (Tremblay and Sinclair 1990a, 1990b). Also on Georges Bank, Gallager © 2001 NRC Canada



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et al. (1996a) found aggregations of ophioplutei below a strong thermocline that occurred between fronts. Increased densities of larvae of several invertebrate taxa (e.g., brachyuran and anomuran crabs, polychaetes, and barnacles) have been recorded in surface slicks at convergences resulting from internal waves (Shanks and Wright 1987). Pineda (1994) found increased densities of crab larvae at convergences of warmwater fronts (indicated by sharp increases in water temperature) associated with internal tidal bores that were passing through rather than ahead or behind the fronts. In a more detailed study, Pineda (1999) showed that larval distribution at such fronts varied among species: cyprids of the barnacle Pollicipes polymerus aggregated at the front, whereas those of Chthamalus had similar abundances at the front as ahead and behind the front; cyphonautes of Membranipora were not found at the front, although they were present both ahead and behind the front. In the laboratory, altered larval distributions in response to the presence of haloclines have been documented for several taxa including echinoplutei (Metaxas and Young 1998a), ascidian tadpoles (Vázquez and Young 1996), barnacle nauplii (Harder 1968), littorinid (Harder 1968) and bivalve veligers (Mann et al. 1991), and decapod zoeae (Sulkin and Van Heukelem 1982). The effects of thermoclines on larval vertical distributions have not been demonstrated as consistently across taxa. For example, thermoclines of >5°C had strong effects on the distribution of echinoplutei (Pennington and Emlet 1986), scallop veligers (Gallager et al. 1996b), and some crab larvae (McConnaughey and Sulkin 1984) but not on that of others (Sulkin et al. 1983). It should be noted that the strong effects in all of these studies were associated with very sharp pycnoclines (i.e., gradients of several degrees Celsius or practical salinity units (psu) over vertical distances of 1–10 cm) that occur in few habitats in the field. Mann (1988) found that oyster veligers readily crossed a halocline with a salinity gradient similar to the one in their natural habitat. Larvae may regulate their position around pycnoclines by modifying their swimming behaviour as they approach the discontinuity. They may remain below or within the pycnocline either by alternating periods of upwards swimming with passive sinking, by swimming horizontally, or by arresting swimming completely and thus remaining at a fixed position if they are neutrally buoyant (McConnaughey and Sulkin 1984; Metaxas and Young 1998a). Mann et al. (1991) showed that upward swimming speed of bivalve larvae increased with increasing salinity in Spisula solidissima and with decreasing salinity in Rangia cuneata, but there was no relationship between downward swimming speed and salinity for either species. A positive relationship between swimming activity and salinity also has been documented for crab zoeae (Sulkin 1984; Forward 1989). These results provide a possible behavioural mechanism for the swimming arrest exhibited by some larvae as they approach areas of decreasing salinity.

Larval distribution around biological features of the water column The distributional patterns of invertebrate larvae in relation to biological features in the water column, such as areas

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of increased concentration of chlorophyll a, have received little attention either in the field or in the laboratory. Scant field evidence suggests that spatial aggregations of invertebrate larvae may coincide with areas of increased concentration of phytoplankton, mainly at or near pycnoclines and fronts. In the Baie de Chaleurs, Québec, Canada, aggregations of bivalve veligers (mainly Mytilus edulis) occurred immediately below the pycnocline and the layer of chlorophyll maximum, but only during the day (Raby et al. 1994). Positive correlations of the concentration of chlorophyll a with larval distribution at night, as well as with a larval feeding index, suggested that diel vertical migration was related to increased feeding in the subsurface layer. In contrast, Tremblay and Sinclair (1990a) concluded that the centre of mass of the distribution of chlorophyll a did not coincide with that of scallop veligers on Georges Bank. However, the vertical distributions in that study show the greatest concentration of larvae at or immediately below the depth of the maximum concentration of chlorophyll a under stratified conditions. Also, on Georges Bank, Gallager et al. (1996a) reported coincidence of high densities of ophioplutei and of diatom colonies of Chaetoceros socialis on a frontal region. In the laboratory, few studies have examined the effect of biological structure of the water column on the distribution of meroplankton. Metaxas and Young (1998b, 1998c) found that echinoplutei aggregated (apparently by choice) either in food patches placed in the middle of a water column or immediately below the patches, depending on algal density in the patch. In experimental microcosms, Gallager et al. (1996b) and Pearce et al. (1996, 1998) found that placing a high concentration of food in the bottom water layer did not override the inhibitive effect of the presence of a thermocline on downward swimming of scallop veligers. Modifications in swimming behaviour that may effect the observed distributions could be manifested through changes in swimming characteristics when larvae are near or in a food patch. While no direct measures of such changes have been published for meroplankton, studies on the response of holoplankton to food patchiness suggest that larvae may also be capable of adjusting their swimming behaviour in response to increased concentrations of food. For holoplankton, certain aspects of swimming and feeding behaviour (e.g., frequency of feeding bouts and jumps, and horizontal displacement) were altered, presumably to allow the animals to remain within the patch (Price 1989; Tiselius 1992). Changes in swimming may arise either as a direct result of physical disruption of swimming (e.g., through particle interference with ciliary activity) or by a behavioural response prompted by mechanoreception of particles by cilia or setae. For example, Molares et al. (1994) alluded to brief arrests in swimming (few seconds) to remove food particles from their setae by nauplii of the barnacle Pollicipes cornucopia. A behavioural response should be evoked by the potential benefit of increased consumption in areas of enhanced food concentration. Hansen et al. (1991) showed that veligers of the gastropod Philine aperta reduced their swimming speed by 40% and increased the radius of the swimming helix in increased concentrations of particles, resulting in enhanced feeding rate. Similarly, holoplankters are known to modify swimming behaviour and patterns of vertical mi© 2001 NRC Canada




gration to enhance feeding rates (e.g., Huntley and Brooks 1982; van Duren and Videler 1995). Detailed descriptions of changes in the swimming behaviour of invertebrate larvae in response to the presence of food are still lacking. Such descriptions would increase our understanding of the role of behaviour in generating aggregations in response to the biological characteristics of boundaries in the water column.

Relative roles of swimming behaviour and hydrodynamics Larval displacement in the water column results from the interactive effects of hydrodynamics (here termed “flow”) and larval swimming (here termed “behaviour”). The flow components relevant to larval displacement are horizontal advection, which results in directed displacement, and turbulent diffusion, which is assumed to result in random displacement and spreading of a group of particles. The slow swimming speeds of invertebrate larvae preclude a behavioural effect on along-stream larval displacement at high flow speeds. However, horizontal flow velocities decrease to near zero at discontinuities such as pycnoclines, possibly allowing larvae to control their displacement as they approach them. Alternatively, larvae may become entrained into a new water layer by the increased turbulence at the mixing interface. Under natural flow regimes in the field, the role of swimming behaviour in larval displacement relative to physical and biological discontinuities in the water column is unclear. Tremblay and Sinclair (1990a) found no evidence that swimming behaviour affected the aggregation of scallop larvae around a thermocline on Georges Bank. Mann (1988) suggested that solely passive dispersal determined the distribution of bivalve larvae relative to a spatially complex frontal system in the James River, Virginia, U.S.A. Similarly, Gallager et al. (1996a) proposed that aggregations of both ophioplutei and diatom colonies near the thermocline on Georges Bank could have resulted from the same physical process, thus indirectly discounting a behavioural mechanism. In contrast, Pineda (1999) suggested that speciesspecific patterns of aggregation at warmwater fronts might be explained by differences in larval swimming ability. He proposed that, unlike barnacle cyprids, the cyphonautes of Membranipora did not aggregate at the front because they are weaker swimmers and could not outswim the downward flows at the convergences that carried them away from the front. Similarly, Shanks et al. (2000) found a concentration of strong-swimming larvae (sergestid shrimps, spionid polychaetes, and crabs) near the seaward surface of a propagating upwelling front, presumably because they can maintain their position relative to the downward flow at the convergence. In the laboratory, the studies that ascertained the importance of behaviour in generating larval aggregations around physical and biological discontinuities in the water column were done under “no-flow” conditions (e.g., Metaxas and Young 1998a, 1998b, 1998c). Thus, the relative importance of behaviour in determining larval displacement under different flow regimes remains relatively unexplored. Swimming behaviour and horizontal advection At large spatial scales (metres to 100s of kilometres), hor-

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izontal advection is the most important factor regulating larval dispersal (for reviews, see Scheltema 1986; Shanks 1995a). Larvae may be advected away from the parental habitat either directly offshore (even across the continental shelf) or alongshore for great distances (Roughgarden et al. 1988). At these large spatial scales, larval transport is mainly the result of hydrodynamics with little contribution from swimming behaviour (e.g., Clancy and Cobb 1997). Similarly, retention of slow-swimming larvae (such as veligers and echinoplutei) within enclosed embayments has been considered passive and attributed to horizontal hydrodynamics (Cameron and Rumrill 1982; Tremblay and Sinclair 1990b). Several mathematical models have predicted larval dispersal and subsequent recruitment using advection by currents as the only process of larval transport (e.g., Jackson and Strathmann 1981; Alexander and Roughgarden 1996). However, a model by Katz et al. (1994) could only predict the observed spatial and temporal patterns in recruitment of American lobster (Homarus americanus) in southern New England, U.S.A., when onshore transport of postlarvae by the dominant currents was coupled with continuous larval swimming. Using another physical circulation model, Tremblay et al. (1994) showed that the transport of larvae of sea scallops on Georges Bank was determined mainly by the circulation pattern, although larval vertical position in the water column (determined by larval swimming) also had an effect on the location of settlement. At small spatial scales (centimetres to metres), little is known about the interactive effects of horizontal advection and behaviour on larval displacement in the water column. Luckenbach and Orth (1992) showed that the swimming speed of megalopae of blue crabs decreased with increasing flow speed in a flow tank. These larvae were capable of swimming upstream when flow speed was < 4 cm·s–1 (and showed bursts in swimming speed as great as 24 cm·s–1 over distances of