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Transitions in morphology, nematocyst distribution, fluid motions, and prey capture during development of the scyphomedusa Cyanea capillata.

Introduction

Trophic impacts of scyphomedusae upon planktonic communities are known to be substantial (Lindahl and Hernroth, 1983; Moller, 1984; Feigenbaum and Kelly, 1984; Behrends and Schneider, 1995), and research on the mechanical basis of prey capture has helped define which constituents of marine planktonic communities are most vulnerable to scyphomedusan predation (Costello and Colin, 1994, 1995; Sullivan et al., 1994; Ford et al., 1997; Suchman and Sullivan, 1998, 2000). However, research on feeding mechanics has focused on adult stages of scyphomedusae, and much less is known about the mechanisms underlying prey capture by the earliest scyphomedusan life stages. An understanding of feeding by juvenile scyphomedusae, or ephyrae, is a prerequisite for an understanding of survival, growth, and planktonic impact of scyphomedusan populations.

Costello et al. (1998) demonstrated that ephyrae spend the bulk of their natural existence actively swimming, and Sullivan et al. (1997) documented the importance of swimming motions for capture of prey by ephyrae. Thus, swimming and feeding appear to be closely related for young as well as adult (Costello and Colin, 1995) scyphomedusae. However, ephyral morphologies are typically different from those of adults of the same species, and consequently, fluid motions and contact between the medusa and its prey may be substantially different for ephyrae than adult scyphomedusae. Although ephyral morphology is strongly conserved among all orders of planktonic scyphomedusae (Russell, 1970; Fig. 1), metamorphosis to adult forms results in highly divergent adult morphologies and associated prey capture mechanisms among the various scyphomedusan orders (Costello and Colin, 1995). Accompanying these changes are important increases in body sizes of developing medusae. For example, Cyanea capillata (Linnaeus, 1758) buds small ephyrae (about 1-4 mm total diameter, Figs. 1, 2) from a diminutive benthic polyp (<5.0 mm body column length). These ephyrae feed in the plankton, subsequently metamorphose, and increase size dramatically on a seasonal basis. Arctic varieties of C. capillata are known to exceed 2.0 m in bell diameter (Russell, 1970) and may therefore undergo a thousand-fold increase in bell diameter during their planktonic life.

[FIGURE 1 OMITTED]

How do developmental changes in size and shape affect prey capture mechanisms used by these scyphomedusae? Because of their smaller sizes and lower swimming velocities, ephyrae experience dramatically different fluid environments compared to adults of the same scyphomedusan species. By virtue of their size, large medusae swim in an inertially dominated flow regime, and entrainment of prey within swimming-induced currents is important for adult feeding (Costello and Colin, 1995). However, the smaller size scale and lower Re flows within which ephyrae exist may inhibit functioning of these same feeding mechanisms. There are two principal reasons for this inhibition. First, momentum, and therefore the ability to transport prey to distal capture surfaces such as tentacles, may not be as influential a component of the lower Re flows surrounding ephyrae. Second, boundary layer thickness increases around structures in lower Re flows (Cheer and Koehl, 1987). As a result, boundary layers surrounding individual morphological elements may overlap to the extent that flow between the individual elements is reduced or absent (Koehl, 1995). In turn, this can limit the effectiveness of morphologies reliant upon sieving prey from flow passing through capture surfaces such as tentacles. Therefore, the small size of ephyrae may inhibit both the flow-based prey entrainment and sieving that have been described for adult scyphomedusae. If so, how does prey capture occur for this widely occurring larval form, and what is the relationship between metamorphic development and the fluid environment of planktonic scyphomedusae?

The goal of this study was to examine these relationships by using a scyphomedusan genus having a cosmopolitan distribution, Cyanea. Our approach partitioned the medusan life cycle into four stages encompassing the ephyral to adult metamorphosis. For each of these stages, we used microvideographic methods to quantify the fluid environment surrounding the medusae (swimming kinematics, particle flow fields) and patterns of prey capture (direct mapping of capture locations). Additionally, we recorded shifts in nematocyst distributions as an aid to understanding ontogenetic shifts in primary prey capture locations. The intention of these different approaches was to provide a basis for assembling emergent patterns of prey capture during metamorphosis of C. capillata.

Materials and Methods

Experimental animals

Ephyrae and medusae were grown in our laboratory (Providence College, Providence, RI) from cultured scyphistomae. These scyphistomae originated from planulae produced by medusae collected in the Niantic River, Connecticut, in a location similar to that of Brewer (1989) and Brewer and Feingold (1991). Newly strobilated ephyrae were maintained at 19 [degrees]C in 0.2-[micro]m-filtered seawater. The ephyrae were fed 3-day-old Artemia sp. nauplii five times per week through development to adult morphology (bell diameter > 1.0 cm). Although the largest size classes that we studied were not yet reproductive, their exterior morphology was similar to larger reproductive individuals. Sexual maturity can occur over a range of bell diameters within a single scyphomedusan species (Lucas and Lawes, 1998; Ishii and Bamstedt, 1998), and we have previously observed gamete production by C. capillata individuals as small as 2.0 cm from the Niantic River (unpubl. data). On the basis of our observations of growth in C. capillata, we partitioned medusan development into four discrete stages. For a description of traits defining these stages, see Table 1. All measurements were made on representatives from each developmental stage. Although the stages allowed comparison of some functional traits during development, they represent snapshots of a continuous developmental process.

Videomicrography

Activities of predator, prey, and tracer particles were video recorded (SVHS) using a backlit optical system (Costello and Colin, 1994). A field counter labeled each sequential video frame (1/60 s per field) to provide temporal information. Spatial characteristics of the optical field were determined from scale bars periodically included in the recordings. Interference from motions in the unmeasured third dimension was minimized by limiting the image depth of field and by selecting particles in the focal plane. The optical system provided clear illumination of particles as well as their movements in relationship to the medusae.

Medusae were recorded while they swam freely in 0.22-[micro]m-filtered seawater within rectangular vessels ranging in dimensions from 4.5 X 8.0 X 2.0 cm to 19.5 X 20.5 X 6 cm (width X height X depth) and volumes from 50 to 1500 ml. Vessel size was influenced by two considerations. First, since only videotape of free-swimming medusae that were more than a bell radius away from the vessel wall was used for analysis, the vessel had to be large enough to allow medusae to swim freely while minimizing contact with walls. Second, image clarity and particle tracking were favored by limiting the depth of the viewing field. The choice of vessel size optimized these factors and depended upon medusa diameter. Capture of 3-d-old Artemia sp. nauplii (0.3-0.6 mm length) by all developmental stages was observed to determine the principal capture surfaces. Individual encounters between medusan predator and Artemia sp. prey were examined frame-by-frame, and the location of each capture was recorded. Capture locations were visible for all major surfaces (lappets, subumbrella, oral arms, and tentacles) during the course of medusan development. Capture of Artemia sp. nauplii was defined as having occurred when contact between the medusa and prey resulted in the prey being held on a medusan capture surface for more than 20 fields (1/3 s). Previous observations had demonstrated that although Artemia sp. nauplii move their appendages extensively, their net swimming velocity is low and they are readily captured and ingested by all stages of Cyanea capillata.

Flow-field quantification relied upon the addition of exponentially growing cells of a large (diameter about 100 [micro]m) diatom, Coscinodiscus sp., to the experimental vessels. These cells were highly reflective and large enough to be tracked in the fluid surrounding swimming medusae. For larger medusae, Artemia sp. cysts (diameter about 300 [micro]m) were used to track fluid motions. Particle paths were collected for a 10-field interval (1/6 s) during the end of bell contraction (power stroke) and continuing into bell relaxation (recovery stroke). Flow fields were constructed from several pulsation cycles because no single cycle contained enough appropriately located and focused particles to describe the entire flow field. We measured the flow field by superimposing an x-y grid on a video sequence of a free-swimming medusa (Costello and Colin, 1994). As the swimming medusa altered orientation, so did the x-y grid, and all particle velocities were measured in relation to the developing bell orientation. Because of greater vorticity in the wakes of larger medusae, particle trajectories became more circuitous as medusae increased in diameter. Calculation of particle displacement distances utilized the net distances traveled over the duration of bell contraction by particles originating near the bell margin at the onset of bell contraction.

Kinematics

All calculations were based upon video recordings of medusae swimming vertically through the fixed viewing frame of a camera. Alterations in bell shape were quantified by the fineness ratio, F, where

F = h/d (1)

and h is bell height and d is bell diameter. F was measured to quantify variations in bell morphology during the pulsation cycle. The fineness ratio of the bell at rest in its uncontracted state corresponds closely to the minimum F value, whereas maximum F corresponds to full bell contraction.

Medusan motion was measured from sequential changes in position (x) of the anteriormost point of the exumbrellar surface over 5-field (1/12 s) intervals (t). Motion only within the two-dimensional viewing field was assured by using a sequence in which bell orientation was level and the medusa swam from bottom to top of the viewing field.

The velocity (u) at time (i) was calculated as an average according to the formula

[u.sub.i] = [[x.sub.i+1] - [x.sub.i-1]]/2t (2)

Reynolds numbers (Re) of the flows around the bell were calculated as

Re = du/v (3)

where u is medusa velocity and v is the kinematic viscosity of seawater.

Nematocyst composition and distribution

Four types of nematocysts were found in Cyanea capillata. Identification was based on the methods of Ostman and Hydman (1997). Homotrichous a-isorhizas were the smallest and most numerous nematocysts identified (7-10 [micro]m in length). Larger A-isorhizas were also present but in much lower numbers. Additionally, as noted by Ostman and Hydman (1997), homotrichous o-isorhizas, heterotrichous microbasic euryteles, and heterotrichous birhapaliods were found over the range of capture surfaces.

Three individuals of each developmental stage were used to document nematocyst type and density. For each individual, replicate nematocyst densities were determined by examining two locations for each of the main prey capture surfaces (lappets, subumbrellar surface, manubrium, and tentacles). Nematocyst counts were based on squash preparations made with a glass slide and cover slip. Tentacles were relaxed following the methods of Ostman and Hydman (1997). A light microscope equipped with an ocular grid was used to determine nematocyst types and densities. A minimum of 100 nematocysts were enumerated for each replicate of each prey capture location.

Results

Growth, morphology, and flow

Development of ephyral through adult stages was accompanied by both growth in size and alterations in morphology (Table 1). Newly released ephyrae possessed a simple, short manubrium, deep clefts between lappets in the bell, and no tentacles. As the newly released ephyrae grew, the clefts between their lappets progressively diminished, the manubrium developed into highly folded oral arms, and elongate tentacles developed (Fig. 2).

[FIGURE 2 OMITTED]

Alterations in size and morphology during ontogeny were accompanied by alterations in the flow surrounding developing medusae. Ephyral bell pulsation, quantified as changes in bell fineness (Fig. 3A), resulted in considerable ephyral activity but little net forward progress because forward motion during bell contraction was largely offset by backward slipping during bell recovery (Fig. 3B). The low maximum velocities achieved by ephyrae (Fig. 3C), in combination with small bell diameters, resulted in Reynolds numbers for the flow surrounding ephyral bells that generally peaked at values near 10 (Figs. 3D, 4). Thus, average Re values for ephyrae were typically lower than 10 and only surpassed this level during peak flow during bell contraction. In contrast, adult medusae experienced some backward slipping during bell recovery (Fig 3F), but their higher velocities (Fig. 3G) and larger bell diameter resulted in significantly higher Re values (average > [10.sup.2], Figs. 3H, 4).

[FIGURE 3 OMITTED]

Flow regimes experienced by medusae changed predictably during medusan development. Maximum Re values, those that occurred during bell contraction, increased throughout the development of the medusae (Fig. 4). Average Re values included periods of bell relaxation (and lower velocities) and were characterized by Re values lower than those for the period including only bell contraction. Maximum Re values occurred during peak flow velocities when prey were often observed to be entrained and captured in flows generated by the swimming medusa. Therefore, while average Re values refer to the general flow conditions around a swimming medusa, maximum Re values provide information about the most rapid flows that are influential for both swimming and feeding by a medusa. Both maximum and average Re for the medusae were closely related to bell diameter because Re is directly related to bell diameter (Eq. 3). Flows around early-stage ephyrae were characterized by maximum Re values of less than [10.sup.1]. However, as the diameter of developing medusae increased, so did Re values, so that medusae greater than 1.0 cm in diameter experienced maximum flows approaching, and sometimes exceeding, [10.sup.2]. Because Re values indicate the relative strength of viscous to inertial forces (Vogel, 1994), early-stage ephyrae experienced flows strongly influenced by viscous forces (average Re < [10.sup.1]), whereas adults experienced flows dominated by inertial forces (average Re > [10.sup.2]). The ontogeny of C. capillata occurred within flow regimes characterized by this shift in the relative importance of viscous and inertial forces.

Flow patterns around developing medusae affected contact between particles transported in those flows and medusan capture surfaces. The region of maximum flow velocities created by bell contraction occurred near the bell margins of all developmental stages (Fig. 5). However, as development proceeded and maximum Re values increased, the distance from the bell margin affected by flow generated during bell contraction, or flow dispersion distance, also increased (Fig. 6). Flows generated by bell contraction of early-stage ephyrae had little effect on fluid in areas more distant than the end of the manubrium (Fig. 5). In contrast, the wake of a swimming adult was characterized by vortices that passed from the bell margin through the tentacles and often impinged on the oral arms (Fig. 5). Intermediate developmental stages were characterized by wake-borne transport of prey over progressively greater (Fig. 6) distances during the power stroke. Therefore, morphological development was accompanied by increased flow magnitude and dispersion.

[FIGURE 4 OMITTED]

Anatomy and prey capture

The relative importance of different anatomical structures used in prey capture shifted during the ontogeny of C. capillata medusae. Ephyral stage medusae (Fig. 7) captured Artemia sp. prey primarily on the manubrium (44%) and bell lappets (35%). The subumbrellar surface was less important (16%), and tentacles are either absent or poorly developed at that stage. The importance of each of these capture surfaces declined through development of the medusae (Fig. 7). In contrast, the importance of the tentacles as capture sites increased, starting with their first appearance in the early tentaculate stage. Rates of development were not completely uniform between individuals, and in some cases a tentacle rudiment formed within 2 days of strobilation during the ephyral phase. As tentacle number and length increased during development, the proportion of prey captured by the tentacles increased from less than 30% to more than 90% by the adult stage (Fig. 7).

Interaction of flow and capture surfaces

Direct observations of Artemia sp. captures indicated that, although all medusan stages entrained prey within flows created during swimming, the process leading to contact with prey differed between ephyral and adult stages of C. capillata. Ephyral bell contraction moved fluid along the exumbrellar surface and bell lappets (Fig. 8; supplementary video at http://www.biolbull.org/supplemental/). Subsequently, bell relaxation drew this fluid into the subumbrellar region near the manubrium on the underside of the lappets. Prey entrained in these flow patterns (Fig. 9) were the principal source of the capture distributions described by Figure 7. Prey were generally entrained during the power stoke when relative animal-fluid velocities are greatest and Re values at their maximum. For small ephyrae, prey captures occurred in relatively viscous flows because prey transport into the subumbrellar region occurred after maximum bell contraction when the fluid flowing around the bell margin, and prey entrained in that fluid, were characterized by maximum Re values [less than or equal to] 10 (Figs. 3, 4). In contrast, prey capture by adult medusae occurred in more inertially dominated (Re > [10.sup.2]) flows (Figs. 3, 4). Consequently, bell contraction by adult-stage medusae resulted in substantially more fluid motion, transport of prey farther from the bell margin, and prey transport into tentacles hanging from the subumbrellar surface of the medusan bell (Fig. 7). As with earlier developmental stages, bell relaxation also drew prey toward the subumbrellar surface of adult stages. Passage of prey-containing fluid through tentacles during both bell contraction and recovery (Fig. 9) resulted in the predominance of tentacles as prey capture sites by adult-stage medusae (Fig. 7).

Nematocyst distributions during development

C. capillata possessed a variety of nematocysts, but a-isorhizas were numerically dominant for all developmental stages and all capture surfaces of each developmental stage. Lesser numbers of euryteles, O-isorhizas, and birhapaloids were found in all stages.

All nematocyst types were combined into estimates of total nematocyst densities to evaluate nematocyst distribution patterns occurring between different capture surfaces and life stages. There were no significant differences in total nematocyst densities between subsamples of capture surfaces or between replicate medusae for each developmental stage (ANOVA, P > 0.6 for all subsample and interindividual comparisons within a developmental stage). Therefore, any differences in total nematocyst distributions were evaluated as reliable indicators of transitions occurring between stages of medusan development.

[FIGURE 5 OMITTED]

[FIGURE 6 OMITTED]

Total nematocyst densities of C. capillata's major capture surfaces altered systematically during medusan development. Nematocyst concentrations on the lappets, subumbrellar surface tissues, and manubrium (termed the oral arms in later developmental stages, Table 1) were greatest for ephyral medusae and declined thereafter as medusae matured (Fig. 10). In contrast, total nematocyst densities of the tentacles were high at their initial appearance in the early tentaculate stage and remained high throughout medusan development. Once the tentacles appeared, nematocyst densities on other capture surfaces declined. These decreases were highly significant (ANOVA, P < 0.001) for the lappets, manubrium, and subumbrellar surface over the course of development from ephyral to adult stages. However, the major differences occurred early in development, during the transition from ephyral to early or late tentaculate stages, rather than during later developmental stages (Fig. 10). Nematocyst distribution patterns stabilized by the late tentaculate stage, and there were no significant differences in total nematocyst densities of any capture surface between late tentaculate and adult developmental stages (Tukey's HSD, comparisons for all capture surfaces between stages, P > 0.5). Therefore, the most substantive changes in nematocyst concentrations of capture surfaces coincided with alterations in flow regimes early in medusan development between the ephyral and early tentaculate stages.

[FIGURE 7 OMITTED]

Discussion

Ontogeny and the fluid environment

With few exceptions, scyphomedusan development entails the transition from a small benthic to a larger pelagic life stage. As with most scyphomedusae, Cyanea capillata's ephyrae arise by fission from a diminutive polyp stage during a process termed strobilation (well described by Russell, 1970). As a consequence of this phylogenetically conserved trait, the physical dimensions of the newly released ephyrae are determined by those of the polyp stage, and ephyrae are typically small (often 1-2 mm, but generally <5.0 mm in bell diameter). This life-history pattern limits scyphomedusae to small initial body size even though adults of species such as C. capillata may be relatively large (>2.0 m in bell diameter, Russell, 1970). Initial growth of ephyrae can be rapid (20%-70% specific daily growth rate, Bamstedt et al., 1999). During this rapid growth period, ephyral weight scales as an approximately squared function of ephyral disc diameter, indicating that bell diameter increases more rapidly than body weight (Bamstedt et al., 1999). This pattern contrasts with adult medusae, for whom weight scales as an approximately cubic function of bell diameter (Bamstedt, 1990; Olesen et al., 1994; Bamstedt et al., 1999). Hence, ephyral growth appears to be allometric and disperses body tissues over relatively wider diameters at less concentrated levels than does the more dimensionally uniform growth of adult scyphomedusae. Due to rapid growth, the ephyral stage is often short-lived in nature, and the transition to adult bell morphologies is generally complete at a diameter of about 1.0 cm. Subsequent growth involves increases in diameter, volume, sexual maturity, and elaboration of structures such as oral arms and tentacles (e.g., Kawahara et al., 2006).

[FIGURE 8 OMITTED]

The relatively rapid increase in diameter compared to mass of developing ephyrae affects bell function during this period. Similarly to adults, developing ephyrae swim nearly continuously under natural conditions (Costello et al., 1998). Although the primary prey capture locations vary during C. capillata's development (Figs. 7, 9), they are consistent with descriptions of flow-dependent prey capture by ephyrae (Sullivan et al., 1997) and adults (Costello and Colin, 1995; Ford et al., 1997; D'Ambra et al., 2001; Dabiri et al., 2005) of other scyphomedusan species. Together, these data indicate that scyphomedusan bells are essential for entrainment of prey in swimming-induced flows through all stages of the scyphomedusan developmental sequence. Despite this similarity in function, the morphological form of the ephyral bell is characteristically different from that of adults (e.g., Fig. 1). Whereas adult bells are most generally continuous discs in outline (See Costello and Colin, 1995, for examples; note that the adult bell of C. capillata has comparatively large lappets), ephyral bells are characterized by thin lappets separated by deep intervening clefts (Figs. 1, 2). The clefts could potentially permit flow between the lappets during both power and recovery strokes of bell pulsation. Substantial flows between the lappets during swimming would result in the bell acting more as a sieve than as a solid paddle, and these alterations in function would have important consequences for both propulsion and feeding by ephyrae. But dye visualizations (Fig. 8 and supplementary video at http://www.biolbull.org/supplemental/) and calculations of inter-lappet boundary layers from kinematic sequences of other scyphomedusan species (K. Feitl et al., University of California, Irvine; pers. comm.) demonstrate that fluid does not pass between lappets at substantial rates during bell pulsation. Instead, fluid flows over the bell margin, allowing the bell to act as a hydrodynamically continuous structure--a paddle--despite the wide clefts between lappets. This combination of discontinuous tissue structure but continuous hydrodynamic function may benefit a life stage that expands more rapidly in its linear dimension, diameter, than it does in organic weight during early development. Mechanical performance of the bell as a paddle is maintained due to overlapping boundary layers around the lappets while organic material allocation maximizes bell diameter increase. In other words, rather than expending organic tissue to fill gaps between lappets that are hydrodynamically continuous anyway, organic material appears to be channeled into rapid growth of the lappets and the central bell disc during early ephyral development.

[FIGURE 9 OMITTED]

This strategy of tissue allocation can be functionally maintained as long as the boundary layers of adjacent lappets overlap during the period of maximum bell velocity. However, as bell diameter increases, so does the Re experienced by the medusa; consequently, the boundary layers become relatively thinner. Thinner boundary layers could result in flow leaking through the clefts in the ephyral bell, but studies of another scyphomedusa, Aurelia aurita, indicate that the central disc expands to fill the inter-lappet clefts with tissue as Re increases during development and boundary layers of adjoining lappets thin (Feitl et al., pers. comm.). Consequently, the early development of scyphozoan ephyrae appears to be a process that maximizes overall bell diameter increase, and tissue is added to the inter-lappet cleft regions only as needed to maintain the hydrodynamic continuity of the bell as a paddle.

A similar economy of tissue investment may underlie the timing of the development of oral arms and tentacles as well as the distribution of nematocysts in prey capture surfaces. Development of oral arms and proliferation of tentacles coincides with the increased ability of the bell to impart momentum to the surrounding fluid (i.e., higher whole animal Re values, Fig. 4) and longer travel distances of particles (Fig. 6) entrained in vortices produced during swimming by larger medusae (Fig. 5). Hence, prey capture structures that trail behind the bell during swimming develop in synchrony with production of increasingly greater fluxes of prey-laden fluid that is transported farther from the bell margin during swimming. We observed most captures of post-ephyral individuals to occur on the tentacles (Fig. 7). This pattern is similar to, but less pronounced than, that for another semaeostome medusa, Chrysaora quinquecirrha, which possesses many fewer, more widely spaced tentacles (Ford et al., 1997). A lower fraction of captures occur on the large oral arms, and one of the major advantages of elongate oral arms may be that they allow rapid removal and digestion of prey intercepting the tentacles. Several studies indicate digestion directly within the oral arms (e.g., Larson, 1986), and the location of the arms near the tentacles is probably quite important for more rapid prey digestion. Although prey digestion rates apparently limit prey ingestion rates of some hydromedusae (Hansson and Kiorboe, 2006), this does not seem to be the case for scyphomedusae. Instead, ingestion rates by scyphomedusae appear to increase linearly with prey concentration over ranges of prey density that greatly exceed those in nature (Clifford and Cargo, 1978; Uye and Shimauchi 2005; Titelman and Hansson, 2006). The rarity of feeding rate saturation in scyphomedusae indicates that clogging of the feeding surface probably rarely limits prey ingestion by scyphomedusae in nature. Instead, limits to prey availability seem to more frequently influence natural scyphomedusan populations (Lucas and Lawes, 1998; Ishii and Bamstedt, 1998). For this reason, maximizing encounter and capture rates is of substantial importance for scyphomedusan populations. We suggest that development of trailing morphological structures in synchrony with increased fluxes of entrained prey at greater distances from the bell margin may allow the developing medusa to maximize encounter and capture of prey in its expanding wake. Although these same morphological structures might contribute to prey capture by the smallest ephyrae, the more viscous, lower Re flows characterizing smaller ephyrae are not as conducive for prey transport to more distant capture surfaces such as elongate oral arms and tentacles. Instead, investment of organic tissue in these trailing structures appears to be limited until the more powerful flows developed in the wakes of larger medusae (Fig. 5) consistently transport prey further from the bell margin (Fig. 6)

[FIGURE 10 OMITTED]

Nematocyst distribution patterns in C. capillata are consistent with the economy of material investment apparent in other morphological developments in this species. Nematocysts are single-use organelles that must be continuously replaced after use. Although the densities that we report are static measures of nematocyst allocation, the combination of nematocyst distribution patterns and capture location maps indicates that the regions of highest nematocyst densities coincide with regions of highest capture frequencies (Figs. 7 and 10). The decline in the nematocyst densities of body regions such as the subumbrellar surface and lappets during development (Fig. 10) corresponds with the decreasing importance of these surfaces for prey capture (Fig. 7) as the fluid regime alters and C. capillata develops more elaborate prey capture surfaces that trail in its wake. It is important to note that although the nematocyst complement remains qualitatively similar throughout development, this does not mean that diet remains constant during development. C. capillata's nematocyst complement shows a wide range of functional characteristics that can be used to capture a variety of prey types (Colin and Costello, 2007). Other variables, such as flow velocities around the bell margin and change with bell size, may affect the types of prey entrained in the wake and therefore available for medusan encounter, capture, and ingestion (Costello and Colin, 1994). Another semaeostome scyphomedusa, Aurelia aurita, expands its dietary range as the diameter of the adult-form medusa increases (Graham and Kroutil, 2001). To our knowledge, no similar data are available for C. capillata, so we do not address changes in prey selection during development. However, our data do indicate that qualitatively similar nematocyst arrays are distributed differently as medusan size increases and that these shifting nematocyst distributions coincide with developmental alterations in wake characteristics and dominant prey capture sites of C. capillata feeding on Artemia nauplii.

We suggest that C. capillata's developmental patterns are strongly linked to the shifting fluid regimes within which medusan development takes place. Although we have distinguished flow by relatively "lower" or "higher" Re values, it is important to recognize that the entire developmental sequence occurs in what is more widely termed intermediate Re conditions (1 < Re < 1000). In this realm, both viscous and inertial forces are important and their interactions can be complex. At the lower end of this range, ephyrae utilize the wide boundary layers characterizing viscous regimes to maintain a hydrodynamically continuous bell surface during swimming. This allows minimal tissue allocation to the inter-lappet cleft spaces and an emphasis on overall diameter increase by ephyrae. Prey is captured via a viscous rebound effect when the contracted bell relaxes and prey-laden fluid refills the subumbrellar cavity. As the developing medusae increase in size and reach the upper range of the intermediate Re realm, viscous forces are less influential and the developmental scheme shifts to one that utilizes the increasingly important inertial forces more effectively. This involves a more materially continuous bell that propels fluid and entrained prey farther from the bell margin to be captured on elongate capture surfaces (e.g., tentacles and oral arms) during both the contraction and recovery strokes of bell pulsation. These latter patterns are maintained as the medusae pass beyond the intermediate Re range and into the inertially dominated realm within which large adult C. capillata function. The synchronous development of morphological features, including even the distribution of the subcellular organelles, nematocysts, represents a highly synchronized interplay between the developing organism and the scale-dependent forces of the surrounding fluid environment.

Application to other scyphomedusae

How universal is the coincidence between hydrodynamic and morphological development among scyphomedusae? Although most scyphomedusae share the ephyral developmental stage (Fig. 1), morphological and prey capture patterns can differ between taxa. For example, Aurelia aurita does not develop tentacles until after the inter-lappet spaces are largely filled in (Russell, 1970; Feitl et al., pers. comm.), and its nematocyst complement differs from that of C. capillata (Purcell, 2003). Additionally, Sullivan et al. (1997) document the lappets as the primary capture location of a variety of prey by A. aurita ephyrae. Therefore, although hydrodynamic conditions are probably similar for all ephyrae due to their small size and low swimming velocities, variables such as nematocyst type and distribution may allow a variety of developmental alternatives that affect the prey capture patterns of different species.

Although adults may differ dramatically, larval morphologies are often conserved by a variety of mechanisms (Raff, 1996). For ephyrae, the biomechanical advantages of lappet-cleft morphologies during the initial period of rapid size increase may be an important factor favoring conservation of the lappet-cleft design. However, the functional advantages of the ephyral design diminish as the medusae develop into the higher Re (>[10.sup.2]) flow environments typical of adult scyphomedusae. In the more inertially dominated environments experienced by larger medusae, a different suite of functional solutions are evident in the wide array of morphologies (Costello and Colin, 1995) that adult scyphomedusae employ for swimming and feeding. Similar studies of the developmental transitions between ephyrae and adult stages of other scyphomedusae will be necessary to determine how representative the patterns found for C. capillata are among other members of the Scyphozoa.

Acknowledgments

The authors are grateful to H. Allen for assistance with early stages of this research. Financial support was provided by the National Science Foundation (OCE 9103309, OCE 0623508 to JHC). The authors thank two anonymous reviewers and S.P. Colin for comments on earlier versions of this manuscript.

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J. E. HIGGINS III (1), M. D. FORD (2), AND J. H. COSTELLO (3,*)

(1) UMS-Wright Preparatory School, 65 N. Mobile Street, Alabama; (2) NOAA / NESDIS / National Oceanographic Data Center, SSMCIII E/OC1 Rm. 4716, 1315 East-West Highway, Silver Spring, Maryland 20707; and (3) Biology Department, Providence College, Providence, Rhode Island 02918-0001

Received 1 September 2006; accepted 1 October 2007.

* To whom correspondence should be addressed. E-mail: costello@providence.edu
Table 1 Morphological characteristics of Cyanea capillata developmental
stages

               Age     Diameter
Stage          (days)  (cm)        Morphological traits

Ephyra           1-3    0.2-0.44   Bell deeply cleft between lappets
                                   Manubrium small and simple
                                   Tentacles generally absent, some with
                                   one tentacle
Early            3-7    0.45-0.64  Clefts between lappets pronounced
  tentaculate                      Manubrium simple
                                   Two tentacles present, rudiments of
                                   others evident
Mid-             7-14   0.65-1.0   Clefts between lappets reduced due to
  tentaculate                      growth of central bell disk and
                                   lappet widening
                                   Manubrium growth and elaboration into
                                   oral arms.
                                   Multiple tentacles extending past
                                   oral arms
Adult          >14     >1.0        Extensive fusion of lappets, clefts
                                   between lappets greatly reduced
                                   Extensive development of oral arms
                                   into sheet-like folds
                                   Many tentacles extending far beyond
                                   oral arms
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Author:Higgins, J.E., III; Ford, M.D.; Costello, J.H.
Publication:The Biological Bulletin
Article Type:Report
Geographic Code:1U6AL
Date:Feb 1, 2008
Words:6535
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