Integrative and Comparative Biology Advance Access originally published online on March 29, 2006
Integrative and Comparative Biology 2006 46(3):312-322; doi:10.1093/icb/icj031
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Good eaters, poor swimmers: compromises in larval form
* Friday Harbor Laboratories, University of Washington 620 University Road, Friday Harbor, WA 98250, USA
School of Oceanography Box 357940 University of Washington Seattle, WA 98195-7940, USA
Correspondence: 1E-mail: rrstrath{at}u.washington.edu
 |
Synopsis |
|---|
Top
 Synopsis IntroductionLarval arms or lobes:...Moving water versus capturing...Different phyla, different...Evolutionary consequences for...References |
|---|
Compromises between swimming and feeding affect larval form and behavior. Two hypotheses, with supporting examples, illustrate these feeding-swimming trade-offs. (1) Extension of ciliated bands into long loops increases maximum clearance rates in feeding but can decrease stability of swimming in shear flows. A hydromechanical model of swimming by ciliated bands on arms indicates that morphologies with high performance in swimming speed and weight-carrying ability in still water differ from morphologies conferring high stability to external disturbances such as shear flows. Instability includes movement across flow lines from upwelling to downwelling water in vertical shear. Thus a hypothesis for the high arm elevation angles of sea urchin larvae, which reduce speed in still water, is that they reduce a downward bias imposed by the vertical shear in turbulence. Observations of sea urchin larvae in vertical shear and comparisons among brittle star larvae are consistent with the performance trade-offs predicted by the model. (2) Structures and behaviors that reduce swimming speed can enhance filtering for feeding. In the opposed-band feeding mechanisms of veligers and many trochophores, cilia push water to swim but movement of cilia relative to the water occurs when cilia overtake and capture particles. Features that may increase clearance rates at the expense of speed and weight capacity include structures that increase drag or body weight and a ciliary band that beats in opposition to the feeding-swimming current. Larval feeding mechanisms inherited from distant ancestors result in different swimming-feeding trade-offs. The different trade-offs further diversify larval form and behavior.
|
Introduction |
|---|
|
Top
SynopsisIntroductionLarval arms or lobes:...Moving water versus capturing...Different phyla, different...Evolutionary consequences for...References |
|---|
Swimming helps planktotrophic larvae move beyond water that they have already processed for food and may help them find aggregations of prey. Swimming and feeding are different processes, however, and there are trade-offs between performance in clearing water of food and performance in swimming. These trade-offs differ among larvae and among environments for the same larvae. Swimming-feeding trade-offs may underlie divergence in form and behavior and differences in preferred habitat.
Here we discuss 2 hypotheses on compromises between swimming and feeding. One hypothesis is that the long arms and lobes that increase maximum clearance rates impair stability of swimming in shear (Grünbaum and Strathmann 2003
). This hypothesis is examined in particular for the pluteus larvae of echinoids (sea urchins) and ophiuroids (brittle stars), but may apply to any larvae with long arms or lobes. The trade-off involves the overall form of the larvae and may explain the reduction or absence of arms or lobes in related non-feeding larvae. The other hypothesis is that there is a compromise between pushing water to swim and creating shear around cilia or setae to feed (Emlet and Strathmann 1985; Fenchel and Ockelmann 2002). This hypothesis is examined in particular for larvae that feed with opposed prototrochal and metatrochal bands (as do many mollusc and annelid larvae) but may apply to other arrays of cilia or setae that both propel the animal and filter particles from suspension.
|
Larval arms or lobes: stability versus speed and weight capacity |
|---|
|
Top
SynopsisIntroductionLarval arms or lobes:...Moving water versus capturing...Different phyla, different...Evolutionary consequences for...References |
|---|
Arms and clearance rates
Diverse larvae capture small planktonic food with bands of cilia. This kind of food is often at low concentrations. To achieve a high rate of ingestion, the larva must clear water of suspended food at a high rate. Clearance rate is the volume of water cleared of food particles per time. The maximum clearance rate depends to a great extent on the length of ciliary bands. One way to support long ciliary bands on a small larval body is to extend the band on narrow arms, tentacles, or lobes. Ciliary bands on arms or lobes are characteristic of the pluteus larvae of sea urchins and brittle stars, the actinotroch larvae of phoronid worms, and the feeding larvae of brachiopods. They occur in some gastropod molluscs, and annelid worms. For all these larval forms, observations of feeding mechanisms indicate that the bands along the arms or lobes are effective in the capture of food particles (Strathmann 1987
). The ciliated arms of the actinula larvae of trachyline medusae may also capture prey. For the echinoderm larvae, maximum clearance rates are proportional to length of the ciliary band (Strathmann 1971; Hart 1996). Feeding currents indicate a similar proportionality for other larvae with ciliary bands on arms or lobes.
Arms and stability
Long arms or lobes might compromise swimming in 2 ways. First, body extensions might compromise stability in shear. Long body dimensions are exposed to greater shear that could change orientation. Second, anteriorly directed arms could shift the center of gravity relative to the center of buoyancy. Most larvae are passively stable so that they swim upward in still water unless they actively change direction. Dense structures positioned posteriorly in larvae confer passive vertical orientation because their center of gravity lies below their center of buoyancy (Fig. 1C) (for example, Pennington and Strathmann 1990; Mogami and others 2001; Fenchel and Ockelmann 2002). In plutei, the anteriorly directed arms (Fig. 1A and B) are associated with a posterior counterweight that maintains a stable orientation (Pennington and Strathmann 1990). The skeleton of arms and the posterior counter weight result in a larval density of about 1.2–1.25 g cm–3 in plutei of a sand dollar, substantially greater than that of seawater (Pennington and Emlet 1986).
|
); angle between arms (ß); center of buoyancy (small sphere); and center of gravity (large sphere). Lateral ciliary bands on each arm are modeled as a tangential velocity perpendicular to the axis of the arm with velocity varying with the cosine of the angle off the plane containing the band (high to low velocities represented here by dark to light shading). For details see Grünbaum (1998). (From Grünbaum and Strathmann 2003Observed swimming in shear
Observations of 8-armed sand dollar larvae (Fig. 1A and B) demonstrated that shear does affect swimming of some armed larvae. In a chamber with vertical shear, the plutei moved across flow lines from the upward current to the downward current (Figs. 2 and 3). The passively stable, upward-swimming larvae moved across flow lines toward downwelling water because they tilted in the direction of least upward velocity. The gradient of velocities was nearly linear across most of the chamber (Fig. 2), and the horizontal velocity of the larvae was approximately constant as they crossed the chamber (Fig. 4). The vertical velocity of the larvae (combined swimming and water flow) changed as they moved horizontally from upward to downward flow. The plutei moved from the upward to the downward current even though they were able to reverse ciliary currents and thus potentially able to maneuver.
|
|
|
The plutei also swam across flow lines from upwelling to downwelling water when they were anesthetized with 1:1 isosmotic MgCl2 and seawater. Anesthetized larvae swim continuously with no reversals and thus swim steadily (Strathmann 1971
). The most obvious difference from unanesthetized larvae resulted from the narrow gradient of velocities near the chamber wall. Drag from the chamber wall produces a narrow velocity gradient, with zero velocity at the wall. On the upstream side of the chamber the anesthetized larvae moved toward the low velocity at the chamber wall. The anesthetized larvae then became "stuck" with arm tips against the wall, held against the wall by their continuous swimming. This did not happen to non-anesthetized larvae, presumably because they reversed ciliary beat and reoriented when they contacted the wall. Anesthetized larvae did not become "stuck" against the wall on the downstream side where maximum downward velocities were less at the wall than a small distance away. That anesthetized larvae swam against the wall on the upstream side but not the downstream side of the chamber is a further demonstration of movement across flow lines toward lower upward velocities: toward the wall on the upstream side but away from the wall on the downstream side. For the sample of all plutei traversing the line of minimum particle motion at the middle of the chamber, 87% of the plutei moved from the upward to the downward current (Table 1). The plutei that did not move across the chamber were those in the fast currents near the chamber walls. Thus passive stability and upward swimming can result in downward transport in vertical shear (horizontal gradients in vertical flow velocities). The mechanism is simple: larvae are tilted toward the slower upward flow or faster downward flow, and their swimming carries them across flow lines.
|
Modeled swimming in shear
Larval features were modeled to examine effect of differences in larval form on performance in swimming (Grünbaum and Strathmann 2003
). The model included number, length, diameter, and orientation of thin, straight, rigid arms. The arms produced a tangential current perpendicular to the axis of the arm (see Grünbaum 1995). The model also included a center of buoyancy anterior to a posterior weight (Fig. 1C). Criteria for performance were upward velocity with no weight and weight capacity (the weight that resulted in zero velocity) in still water and stability in horizontal and vertical shear. These criteria were chosen because many larvae swim upward or migrate vertically (for example, Pennington and Emlet 1990; Young 1995; Fenchel and Ockelmann 2002) and many carry a heavy skeleton, shell, or rudiment of juvenile structures. Speed and stability both affect a larva's ability to change its position in the water column. Shear can reorient swimming larvae, changing the direction of swimming away from the vertical or other preferred orientation. For still water, the results were presented as relative speed or weight capacity. For larvae with the same total arm length, the number of arms had some effect on speed and weight capacity (Fig. 5). Speed and weight capacity decreased as the elevation of arms above the horizontal increased (Fig. 5). Performance in speed and weight capacity was similar over a large range of low arm elevations and declined most markedly at high arm elevations.
|
The results in Figure 5 therefore indicate that low arm elevations and few arms provide the greatest speed and weight capacity in still water. Some ophioplutei meet these criteria, especially at late stages, but many ophioplutei and nearly all echinoplutei do not. In a sample of sea urchin plutei from Mortensen's (1921) plates, 12 of 14 species from 4 orders had postoral arms with elevations greater than 60°, despite a marked decline of speed and weight capacity at arm elevations above 60° (Fig. 5). Transverse portions of the ciliary band between the arms may partly compensate for the disadvantages of these high arm elevations, but why are arm elevations high in so many plutei? One hypothesis for the high arm elevations is problems associated with stability in shear (Grünbaum and Strathmann 2003
). Horizontal shear (vertical gradients in horizontal flow velocities) decreased upward velocity by tilting larvae. With very strong horizontal shear, larvae tumbled. The effect of horizontal shear was least for larvae with many arms at low or high but not intermediate arm elevation angles or with 2 arms at low elevation angles.
Vertical shear (horizontal gradients in vertical flow velocities) resulted in movement across flow lines, just as in the experiment with real larvae. Larvae with high arm elevations were less susceptible to this effect of vertical shear. These results were for larvae with symmetrically distributed arms. Some other arm distributions avoided this effect of vertical shear (D. Grünbaum, unpublished data). However, many plutei have a nearly biradial or radial distribution of arms, like the sand dollar in Figure 1, and these larvae did tilt and move horizontally from upward to downward currents.
Extension to turbulence
The swimming of model and real larvae in vertical shear suggests that turbulence could decrease upward swimming. Though shear in turbulence is in many directions, the vertical component of shear would move the passively stable, upward-swimming larvae toward the downward currents, giving this component of turbulent motion a greater effect. The model indicates that the effect of vertical shear is most pronounced for larvae with low arm elevations (Fig. 6). High arm elevation angles provided greater stability in vertical shear even though they performed less well in regard to speed and weight capacity. Turbulence may contribute to selection for high angles of elevation of pluteus arms, at the expense of lower performance in speed and weight capacity.
|
Predictions compared to larval forms
The model provides an explanation of several features of plutei. Two arms at low elevation angle provide high speed and weight capacity but low stability in vertical shear (Figs 5 and 6). Some ophioplutei approximate this form, with 1 pair of arms much longer than the others and at a low angle of elevation. In a sample of brittle star species from Hendler's (1991) review, the plutei with low elevation of the posterolateral arms are those that retain these long arms as the heavy brittle star juvenile develops (Grünbaum and Strathmann 2003
). The ophioplutei that approximate 2 arms at low elevation appear to be achieving high speed or weight capacity at the expense of stability in vertical shear.
Other ophioplutei and nearly all echinoplutei have high arm elevations. Some plutei compensate for the high arm elevation with horizontal transverse bands between the arms as lobes or epaulettes; some ophioplutei rearrange the band into transverse bands when they become competent to settle and develop rudiments of juvenile structures (Grünbaum and Strathmann 2003).
In most phyla, long arms or lobes of larvae have low elevation angles. Examples include feeding larvae of phoronids, brachiopods, and some gastropods. If the model is an adequate approximation for these larvae, then these larvae achieve greater speed and weight capacity at the expense of stability in vertical shear.
Form is not the only feature affecting stability. Stability can be increased by increased posterior weight (Pennington and Strathmann 1990; Mogami and others 2001), but greater weight increases stability at the expense of speed in upward swimming.
The model predicts that for radially symmetrical arm arrangements, there is no way to simultaneously optimize speed (or weight capacity) and stability in shear. Although real plutei depart from radial symmetry and can reverse ciliary currents, their forms and their behavior in shear are consistent with this prediction. The hypotheses presented by the model need further testing. There are some arrangements of arms, less symmetric, that avoid the transit from upwelling toward downwelling currents (D. Grünbaum, unpublished data). Also, the magnitude of the bias in larval motion from turbulence, as opposed to steady shear, needs to be investigated. Nevertheless, on present evidence, it appears that long arms and lobes increase maximum clearance rate with little investment in ephemeral larval tissues (McEdward 1984, 1986; Hart 1991, 1996), while decreasing stability in shear (Grünbaum and Strathmann 2003). These results help explain the loss of long arms in the transition from feeding to non-feeding larval development in many clades.
Shear and encounters
The model of armed larvae also explained how passive stability results in crossing flow lines in vertical shear. Models in which the organism's swimming is added to the water motion, as in models of effects of turbulence on encounters (for example, Rothschild and Osborn 1988) have not included this consequence of passive stability.
|
Moving water versus capturing particles |
|---|
|
Top
SynopsisIntroductionLarval arms or lobes:...Moving water versus capturing...Different phyla, different...Evolutionary consequences for...References |
|---|
A design criterion for a filter is that water pass through it. A design criterion for a paddle is that water not pass through it. Some arrays of cilia and setae both propel the animal and filter water for food. For some of these animals, there could be trade-offs between swimming and feeding.
Modeling by Cheer and Koehl (1987), Emlet (1988), and Hansen and Tiselius (1992) demonstrates that leakage of water through rows of cilia or setae increases with a greater velocity of movement of the filtering array through the water. Thus moving cilia or setae faster is one way to improve performance as a filter, with water moved per stroke decreasing. Another way to increase leakiness and thus improve performance in filtering is to tether the swimmer. Some flagellates and some pelagic tintinnid ciliates may accomplish this by attaching themselves to larger suspended objects (Christensen-Dalsgaard and Fenchel 2003; Jonsson and others 2004), but attachment is not the only option. Gravity and drag can serve as tethers for pelagic suspension feeders by restraining forward motion (Emlet and Strathmann 1985; Fenchel and Ockelmann 2002). Tethering results in a trade-off between feeding and swimming. When the same structure is being used for filtering and propulsion, tethering enhances filtering while reducing speed.
A third possible means of increasing filtering may be to oppose the filtering ciliary band with another. Veligers of molluscs, many of the annelid trochophores, and entoproct larvae capture particles between parallel ciliary bands that beat toward each other (Fig. 7). The effective strokes of cilia of the prototroch (preoral band) are from anterior to posterior and produce a current for both feeding and swimming. The cilia of the metatroch (postoral band) are shorter than the prototrochal cilia, and they beat from posterior to anterior, toward the prototroch. Although the effective strokes of the prototroch and metatroch thus propel water toward each other, the prototroch produces a current for feeding and swimming because the compound cilia of the prototroch are much larger than those of the metatroch. The prototrochal cilia move faster than particles within the length of their effective strokes; particles beyond the reach of the prototrochal cilia are not captured (Strathmann and Leise 1979; Gallager 1988; Riisgård and others 2000). The inference from these observations is that capture depends on the prototrochal cilia overtaking particles.
|
Hypothesized mechanisms for the capture and concentration of particles include direct interception by a cilium and sieving by more than 1 cilium in the effective stroke (Strathmann and Leise 1979
; Gallager 1988; Riisgård and others 2000). These suggested mechanisms are indirect inferences. The flow of water has not been distinguished from the paths of particles and cilia, and other possible mechanisms need to be explored. For example, the paths of particles captured by sessile animals with opposed bands have suggested other hypotheses, models for capture that depend on the oscillating flow from effective and recovery strokes (Mayer 2001). Mechanisms of ciliary filtration remain speculative, but larval structures and behaviors suggest trade-offs between filtration and swimming. Here we focus on opposed-band feeding, adopt the hypothesis that clearance rates do indeed depend on shear around the prototrochal cilia, and examine the implied trade-offs between feeding and swimming for these larvae.
Emlet (1990) has demonstrated that tethering does affect relative speeds of prototrochal cilia and particles for several larval forms, including one with the opposed-band feeding mechanism. Emlet tethered veligers of the bivalve Crassostrea gigas on a microscope slide and then simulated removal of the tether by supplying a flow equal to the swimming speed. Shear of water around prototrochal cilia was greater for tethered larvae in still water. We examine several ways that larvae may achieve this effect, with a trade-off between swimming and feeding.
Tether to an object
A connection to a large object can completely halt forward swimming and may further increase movement of cilia or setae relative to the water because of drag from the nearby wall. For benthic suspension feeders, the large object is the earth. Ciliary suspension feeders that are tethered to the earth can also increase their capacity to clear particles by orienting to currents (for example, LaBarbera 1977). Though some annelid larvae associate with marine snow (Shanks and Edmondson 1990), we know of no reports of larvae with opposed-band feeding tethering to marine snow, other detritus, or the seabed.
Drag as a tether
Many veligers of bivalve and gastropod molluscs trail mucous strands (Hamner and others 1975; Dobberteen and Pechenik 1987; Hansen 1991; Fenchel and Ockelmann 2002). The strands reduce swimming speed and also change the flow field around larvae (Fenchel and Ockelmann 2002). These larvae feed using the opposed beat of their prototrochal and metatrochal cilia. Presumably, shear around the prototrochal cilia is increased by this mucous sea anchor, enhancing filtration. Fenchel and Ockelmann (2002) compare the volume flows through the prototrochal ciliary band. From velocities of particles upstream from the prototroch, they calculate that the mucous strand increases the volume flow through the ciliated band. In contrast, Emlet (1990) calculated that tethering decreased the overall flux of water past the prototroch, though it increased movement of the cilia relative to the water and thus the volume swept by cilia. We have no explanation for the implied discrepancy in motion of cilia relative to the water but have followed Emlet's observations and analysis in our interpretation of tethering.
Other larvae trail mucous strands but for other reasons than increasing shear around cilia. The feeding annelid larvae that trail mucous strands include chaetopterids and pisionids, which are reported to use the strand itself to catch particles (Werner 1953; Åkesson 1961). Larvae of phyllodocid annelids trail mucous strands (Fenchel and Ockelmann 2002), although phyllodocid larvae do not feed with opposed bands (Strathmann 1987) and may capture particles by other means than filtration. Some larvae trail strands that aid in settlement (Abelson and others 1994).
Weight as a tether
Although a primary function of calcified shells of veligers appears to be defense against predators (Hickman 2001), the weight of the shells may also increase clearance rates at the expense of a slower speed of upward swimming. Gravity can serve as a tether (Emlet and Strathmann 1985). An advantage of mucous strands over shells is that the strands can be shed when speed is needed, but if a larva has a heavy shell, there may be less need for a mucous strand.
An opposed band
The metatroch may be a built-in means of opposing swimming to enhance filtration. The metatroch counters the push of water by the prototroch. It produces a current toward the base of the prototrochal cilia in at least some animals with the opposed-band system (Strathmann and others 1972). If the metatrochal cilia steepen shear gradients around the prototrochal cilia in their effective strokes, then metatrochal beat should increase filtration by the prototrochal cilia (Strathmann 1987). The metatroch does not prevent forward swimming, but its beat may reduce swimming speed.
Some veligers hover when feeding, which suggests that slowing swimming is associated with enhanced filtration for these larvae (Fenchel and Ockelmann 2002). This seems counter to the prediction that arrays of cilia become leakier when the effective strokes are faster (Cheer and Koehl 1987; Emlet 1988; Hansen and Tiselius 1992). One hypothesis is that swimming is slowed by increased beat by the metatroch or changed position of metatroch relative to prototroch during feeding, but observations to test this hypothesis are lacking. Increasing metatrochal beat or producing a mucus strand in response to cues of food availability might reduce swimming speeds when larvae are in good foraging areas relative to their swimming speeds in poor foraging areas. If this occurs, it would be suggestive of an area-restricted search, a foraging strategy known to promote aggregation in resource concentrations in a wide diversity of organisms.
Telotrochs are locomotory bands of cilia near the posterior ends of some larvae, including larval sabellariid worms that feed with opposed bands. Telotrochs and other transverse locomotory bands of cilia propel the larva forward presumably reducing shear around prototrochal cilia. Such specializations for swimming appear to act in the opposite way to metatrochs and may therefore represent compromise between swimming and filtration but in favor of swimming.
|
Different phyla, different swimming-feeding trade-offs |
|---|
|
Top
SynopsisIntroductionLarval arms or lobes:...Moving water versus capturing...Different phyla, different...Evolutionary consequences for...References |
|---|
Different ciliary feeding mechanisms may result in different swimming-feeding trade-offs. Larvae of echinoderms, hemichordates, phoronids, and brachiopods produce feeding currents with bands of simple cilia, usually about 20–25 µm in length. With simple cilia, the flux across a unit length of band is limited; increasing the maximum clearance rate requires a longer ciliary band (Strathmann and others 1972
; Emlet and Strathmann 1994). These larvae thereby become subject to swimming-feeding trade-offs involving arms or tentacles. However, these larvae capture particles on the upstream side of the ciliary band that produces the feeding-swimming current (Hart and Strathmann 1995) and therefore are not subject to the filter versus paddle trade-off.
In contrast, nearly all larvae with opposed-band feeding have compound prototrochal cilia. Grouping cilia into compound cilia permits greater lengths and greater tip velocities in effective strokes. Prototrochal cilia of opposed-band feeders can therefore produce a greater flux of water through a unit length of ciliary band, and maximum clearance rates increase with length of cilia as well as with lengths of ciliary bands (Strathmann and others 1972; Strathmann and Leise 1979; Gallager 1988; Hansen and Ockelmann 1991; Emlet and Strathmann 1994; Henderson and Strathmann 2000). Fewer of the larvae with opposed-band feeding have long lobes. They appear to be less disposed toward instability in shear; however, their filtration is downstream from the cilia producing the feeding current, and these larvae are subject to paddle-filter trade-offs.
|
Evolutionary consequences for larval form |
|---|
|
Top
SynopsisIntroductionLarval arms or lobes:...Moving water versus capturing...Different phyla, different...Evolutionary consequences for...References |
|---|
Instability in shear has implications for the evolution of shapes of feeding and non-feeding larvae. Extension of ciliary bands on arms provides a greater maximum clearance rate. When the requirement for feeding is lost, larval arms are usually reduced or lost entirely (Strathmann 1974
, 1978; Emlet 1995; Wray 1996; McEdward and Miner 2001). Pelagic larvae, even if non-feeding, have functional requirements for swimming. Non-feeding larvae, like the feeding larvae, must avoid predators and settle in favorable habitats, but their ciliated lobes, if present, are short (as in non-feeding larvae of gastropods) or mere vestiges of the arms in ancestral feeding larval forms (as in some echinoids). Arms could be lost because of drift in the absence of selection (Strathmann 1975) or from selection for enhanced performance in swimming by means of transverse rings or broad fields (Emlet 1994). Instability in shear is another possible reason that arms or lobes are commonly reduced or absent in non-feeding larval forms (Grünbaum and Strathmann 2003).
In contrast to larval arms or lobes, modifications that enhance feeding with opposed ciliary bands at expense of forward swimming are not anatomically conspicuous. Many non-feeding spiralian larvae swim with a prototroch and lack a metatroch with an opposed beat, but determining if a metatroch is absent requires close observation. Also, the metatroch may have other functions than capture of food, as suggested by the retention of a reduced metatroch and food groove in larvae of sabellid annelids, which lack an open mouth to ingest food (Pernet 2003). Some larvae with opposed-band feeding can modify the trade-off through behavior, for example, producing or casting off mucous strands or perhaps arresting the metatrochal but not the prototrochal beat (Strathmann and others 1972). Thus there is often little difference in form between larvae feeding with opposed prototroch and metatroch and related non-feeding pelagic larvae.
|
Acknowledgements |
|---|
We are grateful to the Friday Harbor Laboratories and to NSF grants OCE 0217304 (RRS), and OCE 0220284 (DG) for support for this study and to T. Clay, M. F. Strathmann, D. Vaughn, 2 anonymous reviewers, and others for advice. This paper is dedicated to Larry McEdward, the larval marvel.
|
Footnotes |
|---|
From the symposium "Complex Life-Histories in Marine Benthic Invertebrates: A Symposium in Memory of Larry McEdward" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2005, at San Diego, CA.
|
References |
|---|
|
Top
SynopsisIntroductionLarval arms or lobes:...Moving water versus capturing...Different phyla, different...Evolutionary consequences for...References |
|---|
Abelson, A, D Weihs, Y Loya. 1994. Hydrodynamic impediments to settlement of marine propagules and adhesive filament solutions. Limnol Oceanogr 39:164–9.
Åkesson, B. 1961. On the histological differentiation of the larvae of Pisione remota (Pisionidae, Polychaeta). Acta Zool 42:177–225.
Cheer, AYL and MAR Koehl. 1987. Paddles and rakes: fluid flow through bristled appendages of small organisms. J Theor Biol 129:17–39.[CrossRef]
Christensen-Dalsgaard, KK and T Fenchel. 2003. Increased filtration efficiency of attached compared to free-swimming flagellates. Aquat Microb Ecol 33:77–86.
Dobberteen, RA and JA Pechenik. 1987. Comparison of larval bioenergetics of two marine gastropods with widely differing length of planktonic life, Thais haemastomum canaliculata (Gray) and Crepidula fornicata (L.). J Exp Mar Biol Ecol 109:173–91.[CrossRef]
Emlet, RB. 1988. Mechanical models of the opposed-band ciliary feeding apparatus of invertebrate larvae. Am Zool 28:A33.
Emlet, RB. 1990. Flow fields around ciliated larvae: effects of natural and artificial tethers. Mar Ecol Prog Ser 63:211–25.
Emlet, RB. 1994. Body form and patterns of ciliation in nonfeeding larvae of echinoderms: functional solutions to swimming in the plankton? Am Zool 34:570–85.
Emlet, RB. 1995. Developmental mode and species geographic range in regular sea urchins (Echinodermata: Echinoidea). Evolution 49:476–89.[CrossRef][Web of Science]
Emlet, RB and RR Strathmann. 1985. Gravity, drag, and feeding currents of small zooplankton. Science 228:1016–7.
Emlet, RB and RR Strathmann. 1994. Functional consequences of simple cilia in the mitraria of oweniids: an anomalous larva of an anomalous polychaete and comparisons with other larvae. In Wilson, WH Jr, SA Stricker, GL Shinn (Eds.). Reproduction and development of marine invertebrates Baltimore Johns Hopkins University Press pp. 235–57.
Fenchel, T and KW Ockelmann. 2002. Larva on a string. Ophelia 56:171–8.
Gallager, SM. 1988. Visual observations of particle manipulation during feeding in larvae of a bivalve mollusk. Bull Mar Sci 43:344–65.
Grünbaum, D. 1995. A model of feeding currents in encrusting bryozoans shows interference between zooids within a colony. J Theor Biol 174:409–25.[CrossRef]
Grünbaum, D and RR Strathmann. 2003. Form, performance, and trade-offs in swimming and stability of armed larvae. J Mar Res 61:659–91.[CrossRef]
Hamner, WM, LP Madin, AL Alldredge, RW Gilmer, PP Hamner. 1975. Underwater observations of gelatinous zooplankton: sampling problems, feeding biology, and behavior. Limnol Oceanogr 20:907–17.
Hansen, B. 1991. Feeding behaviour in larvae of the opisthobranch Phililne aperta. II. Food size spectra and particle selectivity in relation to larval behaviour and morphology of the velar structures. Mar Biol 111:263–70.[CrossRef]
Hansen, B and KW Ockelmann. 1991. Feeding behaviour in larvae of the opisthobranch Philine aperta. I. Growth and functional response at different developmental stages. Mar Biol 111:255–61.[CrossRef]
Hansen, B and P Tiselius. 1992. Flow through the feeding structures of suspension feeding zooplankton—a physical model approach. J Plankton Res 14:821–34.
Hart, MW. 1991. Particle captures and the method of suspension feeding by echinoderm larvae. Biol Bull 180:12–27.[Abstract]
Hart, MW. 1996. The functional and evolutionary significance of variation in feeding larval forms of echinoderms. Invertebr Biol 115:30–45.[CrossRef]
Hart, MW and RR Strathmann. 1995. Mechanisms and rates of suspension feeding. In McEdward, L (Ed.). Ecology of marine larvae Boca Raton CRC Press pp. 193–221.
Henderson, SY and RR Strathmann. 2000. Contrasting scaling of ciliary filters in swimming larvae and sessile adults of fan worms (Annelida: Polychaeta). Invertebr Biol 119:58–66.
Hendler, G. 1991. Echinodermata: Ophiuroidea. In Giese, AC, JS Pearse, VB Pearse (Eds.). Reproduction of marine invertebrates, Vol. VI, Echinoderms and lophophorates Pacific Grove, CA Boxwood Press pp. 355–511.
Hickman, CS. 2001. Evolution and development of gastropod larval shell morphology: experimental evidence for mechanical defense and repair. Evol Dev 3:18–23.[CrossRef][Web of Science][Medline]
Jonsson, PR, M Johansson, RW Pierce. 2004. Attachment to suspended particles may improve foraging and reduce predation risk for tintinnid ciliates. Limnol Oceanogr 49:1907–14.
LaBarbera, M. 1977. Brachiopod orientation to water movement. 1. Theory, laboratory behavior, and field orientations. Paleobiology 3:270–87.[Abstract]
Mayer, S. 2001. Modelling of ciliary downstream collecting in suspension-feeding invertebrates. Math Meth Appl Sci 24:1409–27.[CrossRef]
McEdward, L. 1984. Morphometric and metabolic analysis of the growth and form of an echinopluteus. J Exp Mar Biol Ecol 82:259–87.[CrossRef]
McEdward, L. 1986. Comparative morphometrics of echinoderm larvae. II. Larval size, shape, growth, and the scaling of feeding and metabolism in echinoplutei. J Exp Mar Biol Ecol 96:267–86.[CrossRef]
McEdward, LR and BG Miner. 2001. Larval and life-cycle patterns in echinoderms. Can J Zool 79:1125–70.[CrossRef]
Mogami, Y, J Ishii, SA Baba. 2001. Theoretical and experimental dissection of gravity-dependent mechanical orientation in gravitactic microorganisms. Biol Bull 201:26–33.
Mortensen, T. 1921. Studies of the development and larval forms of Echinoderms. Copenhagen G. E. C. Gad261.
Pennington, JT and RB Emlet. 1986. Ontogenic and diel vertical migration of a planktonic echinoid larva, Dendraster excentricus (Eschscholtz)—occurrence, causes, and probable consequences. J Exp Mar Biol Ecol 104:69–95.[CrossRef]
Pennington, JT and RR Strathmann. 1990. Consequences of calcite skeletons of planktonic echinoderm larvae for orientation, swimming, and shape. Biol Bull 179:121–33.[Abstract]
Pernet, B. 2003. Persistent ancestral feeding structures in nonfeeding annelid larvae. Biol Bull 205:295–307.
Riisgård, HU, C Nielsen, PS Larsen. 2000. Downstream collecting in ciliary suspension feeders: the catch-up principle. Mar Ecol Prog Ser 207:33–51.
Rothschild, BJ and TR Osborn. 1988. Small-scale turbulence and planktonic contact rates. J Plank Ecol 10:465–74.
Shanks, AL and EW Edmondson. 1990. The vertical flux of metazoans (holoplankton, meiofauna, and larval invertebrates) due to their association with marine snow. Limnol Oceanogr 35:455–63.
Strathmann, RR. 1971. The behavior of planktotrophic echinoderm larvae: mechanisms, regulation, and rates of suspension feeding. J Exp Mar Biol Ecol 6:109–60.[CrossRef]
Strathmann, RR. 1973. Function of lateral cilia in suspension feeding of lophophorates (Brachiopoda, Phoronida, Ectoprocta). Mar Biol 23:129–36.[CrossRef]
Strathmann, RR. 1974. Introduction to function and adaptation in echinoderm larvae. Thalassia Jugoslavica 10:321–39.
Strathmann, RR. 1975. Larval feeding in echinoderms. Am Zool 15:717–30.[Web of Science]
Strathmann, RR. 1978. The evolution and loss of feeding larval stages of marine invertebrates. Evolution 32:894–906.[CrossRef][Web of Science]
Strathmann, RR. 1987. Larval feeding. In Giese, AC, JS Pearse, VB Pearse (Eds.). Reproduction of marine invertebrates. Palo Alto Blackwell Vol. 9: pp. 465–550.
Strathmann, RR and E Leise. 1979. On feeding mechanisms and clearance rates of molluscan veligers. Biol Bull 157:524–35.
Strathmann, RR, TL Jahn, JRC Fonseca. 1972. Suspension feeding by marine invertebrate larvae: removal of particles from suspension by ciliated bands in a trochophore, pluteus, and bdelloid rotifer. Biol Bull 142:505–19.
Werner, B. 1953. Beobachtungen über den Nahrungserwerb und die Metamorphose der Metatrochophora von Chaetopterus variopedatus Renier u. Claparède (Polychaeta sendentaria). Helgoländer Wiss Meeresunters 4:225–38.[CrossRef]
Wray, GA. 1996. Parallel evolution of nonfeeding larvae in echinoids. Syst Biol 45:308–22.[CrossRef]
Young, CM. 1995. Behavior and locomotion during the dispersal phase of larval life. In McEdward, L (Ed.). Ecology of marine invertebrate larvae Boca Raton CRC Press pp. 249–77.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  M. A. Chappell and E. M. Dlugosz Aerobic capacity and running performance across a 1.6 km altitude difference in two sciurid rodents J. Exp. Biol., March 1, 2009; 212(5): 610 - 619. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Calado, G. Dionisio, C. Nunes, and M. T. Dinis Facultative secondary lecithotrophy in the megalopa of the shrimp Lysmata seticaudata (Risso, 1816) (Decapoda: Hippolytidae) under laboratory conditions J. Plankton Res., July 1, 2007; 29(7): 599 - 603. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||