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Settlement in flow: upstream exploration of substrata by weakly swimming larvae.

INTRODUCTION

The behavior of dispersing propagules - juveniles or adults - upon reaching their preferred habitats may play an important role in determining the distribution of species. Most animal species can disperse and select new, favorable habitats as juveniles or adults. However, dispersion of substrate-attached organisms in terrestrial (e.g., fungi and plants) and aquatic (e.g., algae and invertebrates) habitats is accomplished mainly by means of non-motile, or minimally motile propagules carried by external agents. In terrestrial plants, propagules (e.g., seeds and spores) are dispersed by winds or animals, whereas in aquatic organisms, propagules (e.g., spores and larvae) are carried by water flow.

Dispersion via external agents may impose limitations on the selection of favorable habitats. In cases of substrate-attached species, the propagules of which are non-motile, reaching a favorable environment may be largely a matter of chance. Such propagules, for instance, cannot actively select favorable habitats by tracking gradiented settlement cues (e.g., waterborn chemicals). Other substrate-attached species, however, that possess motile propagules, can, after reaching a potential substrate, explore it and, by tracking certain settlement cues, locate a favorable site.

For most benthic marine species, the sole mobile, dispersing stage is the larva, which also has to make the choice of favorable habitat. Larvae of diverse benthic marine organisms are known to select their preferred habitats by responding to various settlement cues, including surface contour (Wethey 1986, Chabot and Bourget 1988), substratum type (Burman et al. 1988), chemical cues (Morse 1990, Pawlik 1992), presence of a microbial film (Strathmann et al. 1981), and flow conditions (Mullineaux and Butman 1991, Pawlik et al. 1991). In addition to its potential role as a settlement cue, flow may also impose hydrodynamic forces that drastically affect, or even prevent, larval active movement, orientation, and maintenance of position relative to the settlement substratum (Jonsson et al. 1991, Abelson et al. 1994). In other words, in those common cases where hydrodynamic forces are much stronger than the forces generated by self-propelled larvae, the larvae may be unable to explore the substratum or to achieve sufficient residence time for establishment of permanent attachment.

Exploration by larvae may play an important role in selecting perceivable cues such as substratum type, substratum topography, and chemical surface properties. Two types of exploration under flow conditions are currently emphasized in the literature: (1) "ping-pong ball" (Keough and Downes 1982) or "balloonist" (Butman 1986) exploration involving repeated vertical movements in the water column alternating with substratum sampling, and (2) drifting with the flow along the substratum (Pawlik et al. 1991). In both cases larvae are carried downstream by the flow. In the first case they may reach the substratum by changing their vertical position; in the second case they drift along the substratum like passive particles transporting as bedload.

Neither of these two types of exploration enables a larva to reach sites that lie upstream from the larva's present position. As a result, where a cue shows a gradual change in the upstream direction, larvae cannot follow this cue in relatively strong currents. Notable examples of such cues are waterborne substances released by conspecific adults (Jensen and Morse 1984), prey organisms (Hadfield and Pennington 1990), and microbial films (Tamburri et al. 1992).

Tracing of waterborne cues, in flow, to their sources cannot be carried out from sites located upstream to the sources. The inability of larvae to move upstream may therefore pose serious limits on the ability of marine species to use cues to locate favorable habitats. Previous studies show that marine organisms downstream from the source can track waterborne tracers in flow (e.g., Weissburg and Zimmer-Faust 1993). Likewise, larvae can respond to waterborne chemicals that mediate their metamorphosis and settlement (Tamburri et al. 1992, Hadfield and Scheuer 1985). Waterborne chemicals from a source in turbulent flow can reach a larva by a combination of advection and turbulent diffusion. As a result, larvae located upstream from the source are unlikely to encounter the cue. To trace chemical sources and other diffusable cues, therefore, larvae must be able to explore substrata against the flow.

Crisp (1995) long ago demonstrated that barnacle larvae can actively move against a relatively slow flow by swimming at 4-5 cm/s (which is fast for larvae; e.g., Chia et al. 1984) and using their adhesive antennules. In contrast, Mullineaux and Butman (1991) reported that barnacle larvae apparently did not explore upstream, especially in the faster flow tested (i.e., 10 cm/s). These contradictory observations, Crisp's unusual experimental setup (which Mullineaux and Butman (1991) noted may not simulate field conditions), and the extraordinary swimming speeds of barnacle larvae (Crisp 1955) raise doubts about the general applicability of Crisp's observations to the larval settlement process. Although there have been some other reports on larval upstream exploration by swimming (Boudreau et al. 1993), to my knowledge, no report exists on larvae exploring upstream in flow velocities that exceed their swimming speeds. The possibility of upstream exploration by settling larvae has thus been virtually ignored in the literature. A recent description of the "... categories of settlement behavior proposed in the literature" by Andre et al. (1993), for example, describes three models of settlement behavior of invertebrate larvae, none of which involves upstream exploration.

The hypothesis here is that certain species that settle in flow, but that may utilize factors other than flow as major settlement cues, should be capable of exploring substrata in any required direction even if the flow imposes hydrodynamic forces greater than those produced by the swimming larva. To examine this hypothesis, I studied the response of cyphonautes larvae of Membranipora membranacea to flow and their exploratory behavior under flow conditions. The response of the larvae to two flow parameters - flow direction and shear (i.e., velocity gradient) - was examined by using two different substratum morphologies (flat plate and cylinder) that induce distinct flow patterns. I chose the cyphonautes larvae of M. membranacea as a case study for two reasons. First, morphological and behavioral studies show that a cyphonautes larva bears a pyriform organ that secretes a thin mucous sheet that aids the larva in locomotion and attaches the larva temporarily to the substratum (Stricker 1988). This feature might facilitate locomotion under flow conditions. Second, M. membranacea prefers the younger, more proximal portions of algal blades (Brumbaugh et al. 1994). Field manipulations suggest that this selective behavior is due to a gradient of unidentified cue on the blade, rather than to the direction of flow (Brumbaugh et al. 1994). In the field the larval response to this gradient is likely to require upstream exploration.

MATERIALS AND METHODS

Experiments were conducted in a simple flow tank to assess the response of settling cyphonautes larvae to shear flow and their behavior in different boundary-layer flow conditions. The settlement experiments were conducted in a circular tank with a stirrer-driven paddle [ILLUSTRATION FOR FIGURE 1 OMITTED]. The advantages of this tank as a tool for larval settlement experiments are (1) its very low volume (1.8 L), which allows experiments to be conducted with only a few larvae, and (2) the non-destructive driving system, which does not harm the larvae during the experiment. The flow generated by this tank is non-uniform and demonstrates a high rate of secondary flows due to the cross-stream recirculation that develops from the stirring at the center of the tank. The location of the settlement substratum halfway between the tank center and walls, however, minimizes the effects of the above phenomenon and prevents wall effect of the tank walls in the vicinity of the substratum, thereby enabling the use of the tank for experiments with localized flows over the substratum.

The velocity range of "mainstream flow" was between 3 cm/s and 5 cm/s (flow velocity of 4.35 [+ or -] 0.85 cm/s [mean [+ or -] 1 SD], n = 13 flow-velocity measurements). Flow velocities were determined from videotape analysis of recorded motion of fine suspended particles 2 cm upstream from the settlement body and between 6-8 cm off the bottom (the height range at which the larval behavior was observed). From the mainstream-flow velocities and the settlement bodies' shapes and dimensions, the ambient flow velocities within the substratum boundary layers (i.e., the actual flow velocities that the larvae experience) were calculated both for the cylinder and flat plate.

Flow direction vs. velocity gradient. - To discriminate between larval response to flow direction and velocity gradient, two substratum shapes were examined in separate sets of experiments: a circular cylinder (1.4 cm in diameter; Reynolds number [Re] = 515 based on diameter) and a flat plate (4.2 cm in length parallel to flow direction; Re = 1544 based on length parallel to flow direction). From Fig. 2 it can be seen that over the cylinder the shear increases with flow direction because the flow accelerates [ILLUSTRATION FOR FIGURE 2B OMITTED]; in contrast, over the flat plate the shear decreases with flow direction because the boundary layer grows [ILLUSTRATION FOR FIGURE 2A OMITTED]. In other words, when moving over the substratum against the flow, the larvae will experience decreasing flow velocities over the cylinder, but over a flat plate they will experience increasing velocities. The substrata were positioned vertically at the tank's bottom a distance of 3.8 cm from the wall and each was covered with a piece of blade of Laminaria groenlandica, an alga known as a favored substratum of M. membranacea. Each blade piece was oriented so that its proximal-distal axis was normal to the flow.

Flow velocities over the cylinder. - The presence of a cylinder disturbs the flow in such a way that the flow accelerates approximately up to the widest cross-section of the body (at [Theta] = 90 [degrees] for a circular cylinder; [ILLUSTRATION FOR FIGURES 2 AND 3 OMITTED]). The tangential velocity of the fluid near the cylinder but outside its boundary layer is equal to [U.sub.[Theta]] = 2[U.sub.m] sin [Theta], where [U.sub.m] is the undisturbed mainstream flow, and [Theta] is the angle from the stagnation point. The outer edge of the boundary layer of a cylinder oriented normal to the flow is defined here as the radial height above the cylinder's surface at which the tangential velocity is 99% of [U.sub.[Theta]]. The factor of 99% defines the accepted, arbitrary fringe between the boundary layer and the free-stream flow. Within the cylinder's boundary layer, tangential flow speed, [U.sub.[Theta]](y), is a function of r, the radial distance from the cylinder's surface

[U.sub.[Theta]](r)/[U.sub.[Theta],m] = f(r[square root of Re]/[R.sub.b]),

where f is a tabulated function, Re is the Reynolds number (based on [U.sub.m] and cylinder diameter) and [R.sub.b] is the radius of the cylinder (Jones and Watson 1963). For r at the edge of the boundary layer (i.e., r = [Delta]), the tabulated function, f, must equal 0.99, for which, according to the tables given in Jones and Watson (1963), r[square root of Re]/[R.sub.b] = 2.4. (In their tables r[square root of Re]/[R.sub.b] is defined as [Eta]). Thus, the boundary layer thickness ([Delta]) of the cylinder is [Delta] = 2.4[R.sub.b] [square root of Re], which is independent of [Theta]. If we assume the velocity increases linearly with r, the velocity gradient along a radius is

dU / dr = [U.sub.[Theta]] / [Delta] = [U.sub.[Theta]][square root of Re] / 24[R.sub.b]

and the ambient velocity ([U.sub.r]) at the level of the cyphonautes larvae ([h.sub.r] = 150 [[micro]meter]) would be

[U.sub.r] = [h.sub.r] dU / dr = 0.015 [U.sub.[Theta]][square root of Re] / 24[R.sub.b],

where [U.sub.r] is the flow velocity at the representative height ([h.sub.r], which is one third of the larval height).

Flow velocities over the fiat plate. - For laminar flow past a plate, the boundary layer equations (Blasius profile) can be solved for [U.sub.r] assuming that the mainstream velocity is constant (Schlichting 1979). The dimensionless velocity profile (u/[U.sub.m]) is a function of the dimensionless variable [Eta](u/[U.sub.m]) = f[prime]([Eta]), or for the flow velocity (i.e., the ambient flow velocity) at the representative height of the larvae ([h.sub.r]), [U.sub.r] = f[prime]([Eta])[U.sub.m], where [Eta] = [h.sub.r] [square root of [U.sub.m]/vx,] x is the distance from the leading edge, and v is the kinematic viscosity (the appropriate f[prime] ([Eta]) for the calculated [Eta] is given in Schlichting [1979]:139: Table 7.1).

[TABULAR DATA FOR TABLE 1 OMITTED]

It should be noted that the flow tank and the measurement methods did not allow direct assessment of the flow velocities experienced by the larvae. However, each of the above calculations underestimated the real flow velocities experienced by the larvae (i.e., average mainstream velocities rather than maximum velocities, relatively low representative height of the larva ([h.sub.r] = 150 [[micro]meter]), and "normal" Blasius profile rather than a profile for an accelerated flow).

Competent cyphonautes larvae were collected from the plankton in San Juan Channel near the Friday Harbor Laboratories (San Juan Island, Washington State) by dragging plankton net with a boat during summer 1994 and were stored in the laboratory in seawater at about ambient sea temperature ([approximately equal to] 13 [degrees] C in late summer) until the experiment. At the start of each experiment, the tank was filled with 50 [[micro]meter] filtered seawater to which the larvae were added. Larvae were offered one suitable substratum. During the experiments, larval behavior was directly observed and videotaped.

RESULTS

Cyphonautes larvae swim with their apical end as the leading part of the body. The locomotion changes when the larva encounters a substratum in either still water or flow conditions. Upon encountering the substratum, the larva crawls on its pyriform organ, which then becomes the leading end of the body. The swimming speeds of cyphonautes larvae are significantly higher than their crawling speeds (Table 1; t test, P [less than] 0.001). No significant differences were found between crawling speeds in different directions (Table 1; ANOVA, P [greater than] 0.439).
TABLE 2. Distribution of cyphonautes larval behavior after encounter
with the substratum in still water and flow conditions.

                                      Exploration
                       Attach-   Per-      With     With
                        ment      pen-      up-     down-
                       without   dicular   stream   stream
                       explor-   to the    compo-   compo-
Water movement          ation      flow     nent     nent     Total

Still                     0          -        -        -       42
Flow over flat plate      0          1       28        9       38
Flow over a cylinder      0          3       38        1       42


None of the larvae permanently attached themselves at the first site encountered on the substratum. Instead they began moving over the substratum surface while adhering to it with mucus secreted by the pyriform organ (I have termed this type of locomotion "crawling," although the exact mechanism is unknown, but it is not likely to be crawling in the classical sense). The surface exploration took place in various directions, but exploration with an upstream component was significantly more frequent than in other directions (Table 2; G test for goodness of fit, P [less than] 0.005 on the flat plate, P [less than] 0.001 on the cylinder). On the cylinder, larvae moved against the flow until they reached the stagnation point ([Theta] = 0 [degrees]) where they moved axially up or down. On the flat plate, the larvae moved upstream towards the leading edge (x = o) and either moved along it, stayed in one spot, dislodged, or went to the other side of the plate, A comparison between the flow velocities experienced by the larvae and maximal larval locomotion speeds showed that cyphonautes larvae can move under much higher flow velocities than their locomotory speeds (either swimming or crawling; [ILLUSTRATION FOR FIGURE 3 OMITTED]).

DISCUSSION

Many studies have examined the active response of larvae to settlement cues. A common description found in such studies is that larvae explore substrata by swimming or crawling before selecting an appropriate site for settlement, evidently by sensing the relevant cue examined in the particular study (e.g., Rittschof et al. 1984). However, the vast majority of settlement-cue studies designed to investigate site selection by larvae were conducted in still water, which enables all motile larvae, including the extremely slow ones, to move in any direction along gradients of environmental parameters. In nature, larvae of many species settle in sites with flowing water. Under realistic conditions, flow is known to affect active selection of an appropriate site through the influence of the hydrodynamic forces on the settling larva (Butman et al. 1988, Jonsson et al. 1991, Abelson et al. 1994). Despite this known fact, only very few studies have been conducted to assess the combined effects of settlement cues and flow (e.g., Butman et al. 1988, Pawlik et al. 1991). These studies have suggested that site selection may be determined largely by a cue other than flow, but that flow may also influence selection by exposing larvae to sites for perusal.

Motile larvae arriving at a substratum under low flow velocities are able to explore while swimming or crawling over the surfaces and, after selecting an appropriate site, are able to achieve sufficient residence time to establish permanent attachment. However, it has been assumed that when the current is faster than the larva's swimming speed, hydrodynamic forces prevent it from exploring the substratum freely in all directions or achieving residence time for attachment. A mechanism for attachment in fast flows, however, has been suggested for coral larvae (Abelson et al. 1994). These larvae secrete mucous threads with which they instantaneously attach to substrata in flow, presumably to maintain their position in one spot. In the present study, cyphonautes larvae were also found to use mucous threads for the initial encounter and attachment. Work with larvae of hydrozoans and tunicates (T. Newberry, C. Lambert, and A. Abelson, unpublished data) and a literature survey (A. Abelson and M. W. Denny, unpublished manuscript) reveal that such a solution may be widespread across benthic taxa. The disadvantage of this type of instantaneous-attachment mechanism is that it could prevent larvae from executing the exploration phase. Some larvae can overcome this disadvantage by detaching themselves from the substratum and returning to the flow, when they encounter an unfavorable substratum. In such a case, however, the larva has to leave the substratum, and will be unable to explore any substratum that is situated in strong flow. If exploration is required, this will necessitate devices that enable the larva to move while still maintaining its attachment to the substratum (i.e., "adhere and explore" mechanisms).

The present study shows that larvae are not necessarily restricted to points of initial encounters, or to exploration only in the downstream direction. Cyphonautes larvae are able to explore substrata under flow velocities that are much higher than their locomotory speeds. Although, the adhere-and-explore mechanism of the cyphonautes larvae is not yet clear, the larvae have been observed to use their pyriform organ to secrete mucus by which they attach to the substratum while moving forward. The cyphonautes larvae thus provide an excellent example of weakly swimming larvae that are able to move in any desired direction under flow velocities much faster than their measured locomotory speeds. I suggest that the exploration behavior observed here is not restricted to cyphonautes larvae alone. Another possible example is exhibited by cypris larvae of barnacles, which utilize their antennular attachment organs to fasten to the substratum while they explore it (e.g., Yule and Walker 1984, 1987). Although the role of these organs as an adhere-and-explore mechanism has not been studied in the context of cypris behavior under flow conditions, it is very likely that the temporary adhesion function of these organs assists the larvae's explorations under flow conditions. This mechanism of the cyprid larvae might explain deviations of settlement distribution from encounter distributions of barnacles under flow conditions (as found by Walters 1992).

Larval response to flow should be separated into response to flow direction and to shear (or velocity gradient). The importance of flow direction lies in the convection of suspended or soluble matter. Shear has been described for its constraining role in preventing larvae from attaching to the substratum, or dislodging already-attached larvae (Eckman et al. 1990, Pawlik and Burman 1993). Crisp (1955) argued that the velocity gradient close to the substratum is the parameter of flow that affects the attachment of larvae of sessile species, whereas the nominal speed of the water is important only for its influence on the velocity gradient. In the same study, however, when referring to the "migration behavior" (i.e., exploration) of larvae before attachment, Crisp related larval migration to flow direction rather than to the velocity gradient. Moreover, the experimental setup in Crisp's study did not enable discrimination between larval response to flow direction and velocity gradient.

The results of the present study show that cyphonautes larvae favor exploration in the upstream direction on both substratum types (flat plate and cylinder). Therefore, flow direction - rather than the velocity gradient or boundary shear stress - appears to be more important in directing the cyphonautes larva's exploratory locomotion. This behavior may match the site-selection process of cyphonautes larvae in the field, where larvae preferentially settle on younger, proximal portions of kelp blades. In the field, proximal portions of blades lie upstream, so that upstream exploration should lead the larvae to these portions, and can be used as a secondary but reliable settlement cue. In contrast, the increasing velocity gradient may change directions due to non-uniform surface contour, typical to many algal blades, and therefore cannot reliably lead the larvae to the proximal portions.

Upstream exploration by weakly swimming larvae is probably more common than is currently assumed. It is probable that such larvae employ adhere-and-explore mechanisms that enable them to control their position, to move in all directions, and to achieve the residence time necessary for permanent attachment in relatively strong flow conditions. By enabling upstream exploration, the adhere-and-explore mechanisms can promote tracking of waterborne chemicals to their source. In a recent study, Turner et al. (1994) demonstrated settlement enhancement of oyster larvae by water-soluble chemical inducer (i.e., cues) in flow. The authors also suggested that the enhanced settlement follows from a quick response of the larvae (i.e., downward swimming) to low concentrations of the chemical inducer, rather than by larval travel towards higher concentrations. Although such a mechanism may allow effective settlement of species able to tolerate a wide range of environmental conditions, it is unlikely that such a mechanism can act as a reliable method of habitat location for species that are confined to spatially limited, specific sites (e.g., obligatory host organisms). The chances of larvae directly encountering such spatially limited sites are extremely low, whereas settling and metamorphosing in downstream locations that lie within the metabolite plumes of these sites appears impractical. For such species, upstream exploration may dramatically increase the chances of locating the potential sites by utilizing the sites' spacious odor plumes.

ACKNOWLEDGMENTS

I thank C. A. Butman, M. Denny, T. Newberry, R. Strathmann and anonymous reviewers for instructive criticism on the manuscript. I also thank R. Strathmann and the director and staff of the Friday Harbor Laboratories for their hospitality and use of facilities. This research was supported by Fulbright junior scholarship of the USIEF and the Ben-Gurion Post-doctoral fellowship of the Israel Ministry of Science.

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Date:Jan 1, 1997
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