flow and polypide distribution in the cheilostome bryozoan bugula and their inference in archimedes

Flow and polypide distribution in the cheilostome bryozoan Bugula and their inference in Archimedes FRANK K. McKINNEY, MONICA R. A. LISTOKIN AND C. DAWN PHIFER

McKinney, Frank K., Listokin, Monica R. A. & Phifer, C. Dawn 198601 15: Flow and polypide distribu-

Oslo. ISSN 0024-1164.

Cilia-generated flow in the absence of ambient current is directed from frontal to reverse sides of branches in Bugula turrita, B. turbinata, B. neritina, and B. stolonifera, whether axes of feeding lophophores are perpendicular to the basal plane of branches or are tilted toward distal ends of branches. Ambient current less than 5 cm per second interacts with cilia-generated flow, but ambient flow of 15 cm per second de- stroys self-generated colonial flow and severely hampers feeding. Polypides are located in the more distal, younger portions of colonies, in species with and without polypide recycling, whereas zooids in the more proximal, older portions are senesced. Presence of feeding polypides in distal but not in proximal portions of the larger spiralled colonies of B. turrita and B. turbinata results in downward, slightly radially directed flow through the colony. The colonial flow passes directly from one whorl to the next-proximal so that water exits from low around the colony perimeter, and a proximally expanding conical stagnant zone occupies the interior of the colony. A substantial percentage of zooecia in distal whorls of well-preserved Ar- chimedes is filled by sediment and inferred to have been occupied by actively feeding polypides. whereas spar-filled zooecia capped by terminal diaphragms were apparently senesced during the latter part of a colony’s existence. The capped zooecia constitute an increasing percentage of the total in more proximal whorls. Generally similar colony form and inferred similarity in distribution of current-generating polypides in spiralled colonies of Bugula and in Archimedes suggest that colony-generated flow in Archimedes was similar to that in Bugula, passing downward and then outward, and only through the distal whorls of the colonies. 0 Bryozoa, feeding currents, spiral growth, senescence, Cheilostomata, Fenestrata.

Frank K . McKinney, Department of Geology, Appalachian State University, Boone, North Carolina 28608, U.S.A., and Research Associate, Field Museum of Natural History, Chicago, Illinois; Monica R. A . Lis- tokin and C. Dawn Phifer, Department of Geology, Appalachian State University, Boone, North Carolina 28608, U.S.A.; 3rd April, 1985.

LETHAIA tion in . the cheilostome bryozoan Bugula and their inference in Archimedes. Lethaia, Vol. 19, pp. 81-93.

The first description of colonial water flow patterns in bryozoans was for the purpose of inferring function of surface texture of robust fossil bryozoans with large, continuous surface areas (Banta et al. 1974). Subsequent papers on colonial water flow patterns in bryozoans have dealt with description of flow patterns seen around living bryozoans (Cook 1977; Winston 1978, 1979; Lidgard 1981; Nielsen 1981) or with hypotheses about flow around fossil bryozoans (Taylor 1975, 1979; McKinney 1977; Anstey 1981). With the exception of Winston (1981), there have been minimal comparisons of directly observed flow in living colonies and inference of flow in analogous fossil forms by the same investigator.

The purpose of this paper is to consider water flow patterns through two morphologically very similar growth forms (Fig. l ) , living colonies of spiralled species of the gymnolaemate Bugula and colonies of the Palaeozoic stenolaemate Ar- chimedes. In this paper, inference of flow through Archimedes is based on observation of flow through living Bugula colonies and on com-

parison of colony morphologies and probable polypide distributions. We consider that Bugula is not only a general morphological analogue of Archimedes, but that patterns of water flow around and through Bugula colonies are the most dependable guide available for inferring water flow for Archimedes.

Previous work The apparently earliest published hypothesis on water flow through Archimedes colonies was by Yakovlev (1923), who wrote: ‘A very original body form occurs in the Carboniferous bryozoan Archimedes, where the platelike body of the colony is extended in a vertical direction and twisted in a spiral analogous with Archimedes’ mechanical screw o r screw-cutting machine. No doubt this adaptation makes water successively pass through the entire body from below to above, so that the supply of nourishing matter will be fully utilized’ (column 56, translation by

6 Lxthaia 1/86

82 Frank K . McKinney and others

F.K.M.). It is not clear whether Yakovlev thought that water passed upward between branches and through the fenestrules, or that the water flowed upward in a spiral motion, confined to the continuous spiral slot defined by adjacent whorls of branches.

Condra & Elias (1944) interpreted Yakovlev’s statement to mean that ‘the current which sup- plied the food must have followed the coiling, that is, it was a whirlpool or vortex’ (p. 37). They elaborated on this concept and considered that the concerted action of ciliary movement in thou- sands of polypides within a colony drove a cur-

LETHAIA 19 (1986)

Fig. I . Paleozoic and Recent erect spiralled bryozoans. Bar scales indicate approximately 5 mm. 0 A . Archimedes infer- medius (Ulrich). Basal calcareous shale facies of Bangor Limestone (Chesterian; Visean-Namurian), Fox Trap, Col- bert County, Alabama. Field Museum of Natural History (FMNH) PE39305. 0 B. Eugula furrifa (Desor). Woods Hole. Massachusetts: noncurated specimen.

rent that ‘moves along the obverse (frontal surface) of the colony from the base toward the distal part and tends to be weaker at the sides’ (p. 41). They thought that the current was most vigorous in the midst of the area between colony axis and branch tips, thereby allowing axial and marginal skeletal structures to thicken. In addition, they hypothesized that the apical vortex where the current escaped the colony was re- sponsible for maintaining a rotational stress on the growing apex of the colony.

As had Condra & Elias (1944), Cowen & Rider (1972) lamented the lack of observations

LETHAIA 19 (1986) Flow and polypide distribution in BUCULA 83

on colony-generated flow around living bryo- from the northeast of Ile Callot, Morlaix Bay zoans. However, they hypothesized water flow near Roscoff, France, by G. Lutaud. Colonies through Archimedes colonies based on (1) known spanning the range of sizes available in the col- direction of cilia-generated flow through individual lophophores of living bryozoans, (2) a concept of transversely truncated distal ends of the spiralled colonies, and (3) the apparent presump- tion that all zooids were alive and capable of feeding except those imbedded in the massive skeleton of the central screw-shaped support. Cowen & Rider envisioned water currents, driven by ciliated tentacles of lophophores, pas-

lection were dissected by cutting the axial margin between origins of successive, radiating branch systems. Each branch system was examined wet in 70% ethanol with transmitted light, distributional patterns of the clearly visible polypides and brown bodies were recorded, and percentage of total zooids that are polypide-bearing in each branch system was calculated.

Living colonies of Bugulu neritina and B. stolo- sing downwards through fenestrules from frontal to reverse surface of each whorl, with two major components to colony-wide flow. They hypothesized a downwardly spiralling current that was

niferu were collected from Bogue Sound, North Carolina, and observed in the University of North Carolina's Institute of Marine Sciences, Morehead City. The colonies were observed at

set up from the broad -surface of an incomplete cone formed by the uppermost whorls of branches, with inner zooids of each whorl pump- ing through fenestrules and feeding from some portion of the spiralling water so that it was nutrient-poor when it reached the colony base. In addition, Cowen & Rider conceived of an inwardly-diminishing flow of water over the frontal surface of each whorl, because each feeding zooid diverted part of the inwardly flowing water through fenestrules, and most of it flowed back out along the reverse surfaces of the same branches, above the inwardly-flowing water of the next-proximal whorl.

Yet another concept of flow in Archimedes

magnifications of x10 to x50 in 0 to 15 cm per second ambient current in a recirculating Vogel- LaBarbera flow tank (Vogel & LaBarbera 1978). Milk and naturally-occurring silt and organic detritus served as current tracers. Videotapes were used to accurately document current patterns through colonies at varying ambient current velocities.

Living colonies of Bugulu turrita from Woods Hole, Massachusetts, were obtained from the Marine Biological Laboratory and examined at Appalachian State University. The vigorously feeding colonies were observed in still to gently agitated water, 24 to 72 hours after collection. Silt and organic detritus in the water in which the

colonies was provided by Anstey (1981), who colonies were maintained was resuspended and conceived of water entering the colonies between served as current tracers. Other colonies were whorl levels, where it was then filtered by lopho- fixed immediately upon collection, preserved in phores of the underlying branches. But rather 70% ethanol, and were examined for occurrence than filtered water passing through fenestrules, it of polypide-bearing zooids as described for B. travelled along branch surfaces inwardly to the turbinutu. spiralled skeletal axis, which eventually delivered Archimedes specimens that were used for the all the filtered water from the colony to the sub- study belong apparently to A . intermedius (UI- stratum at the base of the spiral. According to rich) and were collected from the lower marly- Anstey's hypothesis, the water travelling along weathering calcareous shale of the Bangor Lime- branch surfaces towards the colony axis would stone (Chesterian; Upper Mississippian), Fox have generated hydraulic lift that could have Trap, Colbert County, Alabama. We used only a caused a slow upward drift through the fenes- few essentially complete samples drawn from a trules.

Materials and methods

collection of several thousand variably complete specimens. They were sawn down the middle, and the better centered of the two resulting faces was polished, etched, and replicated by acetate peel (Boardman & Utgaard 1964). After the ini- . . -

Specimens of Bugulu turbinutu for this study are alcohol-preserved and were fixed soon after collection, before deterioration of the colonies. They were collected in 1971 and 1980 from rock substrata in the low intertidal from Brest and

tial surface was replicated, the specimen was ground down a total of about 0.3 mm in two stages, and additional sets of acetate peels were made. Each zooid in one side of each whorl level in each specimen was scored for (1) partial or

6'

84 Frank K . McKinney and others LETHAIA 19 (1986)

in number from a central axial region. The axial region of the colony was heavily calcified and constituted a central screw-shaped support structure. Additional colony strength was generated by dissepiments, which are skeletal structures that link adjacent branches, and by secretion of a narrow but continuous skeletal band along outer whorl margins in proximal regions.

Spiralled Bugula colonies consist of narrow, flexible, lightly calcified unilaminate branches that radiate and increase in number from a central axial region. The axial region of the colony lacks any structurally strengthening material beyond the typical lightly calcified cuticle found throughout the colony. Branches are not laterally linked, and colonies are unrestrictedly supple from branch tips to colony base except where fouled by other organisms.

In Bugula and Archimedes, branch widths are between 0.25 and 0.50 mm, spacing between adjacent branches is about equal to branch width, branches are arranged in whorls that originate and radiate from a helical colony margin that constitutes the colony axis, whorls are inclined about 60 degrees from the apical end of the colony axis, and spacing between whorls is typically a few millimeters. In both taxa, each whorl is composed of a few systems of bifurcated branches, and each system originated from a branch developed at the rapidly bifurcating axial colony margin (McKinney 1980, 1981). Whorl diameter in both diminishes toward the apical tip of colonies (Fig. l ) , giving an inverted conical shape to the apex. Growth habits and colony form are so similar in Archimedes and spiralled Bugula that their colony forms may be generated with precision by a single simulation program, and they occupy only a very small portion of the the- oretical morphospace available (McKinney & Raup 1982).

Fig. 2. Preservation states of zooecial chambers in branch p ~ r - tions beyond the heavily calcified axial screw in Archimedes in- rermedius (Ulrich). Locality as in Fig. 1. Bar scale equals 0.5 mm. FMNH PE39306. 0 A. Zooecial chambers in a distal whorl, those in center and left partially mud-filled, and spar- filled chamber on right capped by thin terminal diaphragm. 0 B. Spar-filled zooecial chambers capped by thick terminal diaphragms in a proximal whorl.

complete mud filling of the zooecial chamber, (2) presence of lamellar terminal diaphragms, or (3) a planar boundary at zooecial apertures between the surrounding mud matrix and the sparry infil- ling of zooecial chambers (Fig. 2). The mud-containing zooecial chambers were interpreted as open and possibly containing a polypide at the time of colony death; the other two states were interpreted as nonfunctioning zooids at the time of colony death. Distributional patterns of mud- containing versus spar-filled chambers, and percent of mud-containing apertures per whorl level were recorded.

Spiralled structure of Archimedes and Bugula Archimedes colonies consisted of narrow, rigid, unilaminate branches that radiated and increased

Flow through Bugula colonies Live colonies in quiet water. - All flow through Bugula colonies in quiet water is generated by movement of lateral cilia on tentacles of expanded, feeding lophophores. In B. neritina, zooids are arranged biserially in alternating posi- tions along branches, and protruded bell-shaped lophophores (Fig. 3A) near the ends of branches are capable of moderately agile scanning atop long extroverted tentacle sheaths. They are tilted a few degrees laterally and distally so that a scant


Fig. 3. Current-generating. feeding lophophores in species of Eugula. Bar scales indicate approximately 1 mm. 0 A. Eugula neri- tino (Linnaeus). Bogue Sound, North Carolina. 0 B. Eugula stolonifera Ryland. Bogue Sound, North Carolina. 0 C. Eugula turrita (Desor). Woods Hole, Massachusetts. 0 D . Eugula turrifa (Desor), distal tip of colony. Woods Hole, Massachusetts.

majority of their area is over the space adjacent to the branch and the smaller portion is above the branch. The current generated by lateral cilia passes from the frontal region through the spaces between tentacles, then through the region behind the lophophores, and finally to the region behind the branches, where its momentum is lost. Current-tracing veils of milk that drift toward frontal surfaces of branches may suddenly be perforated by inwardly tapering cylindrical columns of water drawn into lophophores from distances up to 2 to 3 mm, with a thin, gradually tapering, funnel-shaped film of milk defining the column right to the level of intersection with the tentacles of the lophophore. Gradually the entire

veil of milk is drawn to the level of the semi- planar branch systems that are composed of several adjacent, subparallel branches, and the filtered water is all forced through the slots between branches to the region on the reverse side.

The colonies observed were so efficient at clearing milk that water movement could not be traced after passage through lophophores. How- ever, the complete paths of rejected silt and detritus particles may be clearly seen (Fig. 4). In still water, particles are drawn towards the colonies, along with the water from above the frontal side of the colony. The particles increase in velocity as they approach the functioning lophophores, through which they travel at about 5 to 6


Fig. 4. Trajectories of individual particles of detritus travelling in cilia-generated flow through a colony of Bugula neritina.

mm per second. The particles and water then are passed through the slots between branches, to the reverse side, where they continue moving perpendicularly away from the branches. Move- ment perpendicularly away from the branches is maintained for a distance of several mm regard- less of their orientation, except where branches are inclined and gravity gives a vertical com- ponent to movement of some of the coarse silt and fine sand particles.

Actively feeding polypides occur in up to seven zooid lengths in the outer tips of branches in the colonies that we observed. In more proximal regions, zooids are regressed and lack functional polypides. In Bogue Sound, these proximal parts of colonies are heavily fouled, which suggests that the feeding function is lost a short distance behind branch tips, with perhaps only one polypide generation being typical.

B. stolonifera also consists of dichotomously divided biserial branches with alternately placed zooids; conical, bent-tentacle lophophores that are spread at about a 45 degree angle; and short introverts (Fig. 3B). Branches are less flexible than those of B. neritina. Polypides are present

0 1 mm - within zooids for a greater distance proximally than in B. neritina, although the older, central and basal portions of large colonies generally lack polypides except in a very few zooids. Cilia- generated flow through B. stolonifera colonies resembles that in B. neritina; water is drawn from areas frontal of branches, is filtered by lophophores that protrude partially over branches and partially over spaces between branches, and passes to the reverse sides of branches, where its motion becomes less directed and well defined. Al- though as in B. neritina some lophophores have their axes inclined distally, filtered water passes between branches, perpendicularly to the local plane of the branch system.

Zooids of B. turrita alternate from side-to-side in biserial, dichotomously divided branches. Pro- truded lophophores are high, conical and are densely crowded over the frontal surfaces of regions where zooids contain polypides (Fig. 3C). Introverts are relatively short, and axes of lophophores are inclined distally with respect to branch growth direction so that they are roughly parallel with the colony axis or are tilted slightly away. The position of lophophores when protruded is

LETHAIA 19 (1986) Flow and polypide dktribution in BUGULA 87

l e 3 4 S c ; i B Whorl number

Fig. 5. A. Percent zooids per whorl occupied by polypides in four colonies of Eugulu furrifu and one of E . plumosu (Pallas). 0 B. Diagrammatic longitudinal section of E. furrifu showing distribution of polypides (stippled bars) and downward, obliquely centrifugal flow surrounding interior stagnant region.

relatively inflexible, with no or very little lateral adjustment or ‘scanning’, although closure from the expanded state to a temporary, narrow conical cage shape is common.

At the distal tips of colonies (Fig. 3D), cilia- generated currents draw water directly from the region distal to the tip, toward and through the lophophores. The filtered water continues between the branches, then continues toward those in the next-proximal whorl, travelling in a direction almost normal to the branches. Water that enters the apex of the colony therefore passes through several whorls of branches. The 60 degree angle between colony axis and the whorls results in the water being directed radially away from the axis and exiting the colony laterally after passing through only a few whorls (Fig. 5B). The portion of any whorl that projects beyond the overlying branches within the distal, tapered part of the colony also draws water new to the colony from the region around the perimeter of the overlying branches. It too is added to the water that is moving down and slightly centrifugally through the colony to the point where it flows out laterally. The interior of the colony is occupied by a conical region of stagnant water whose apex

is 3 or 4 whorls proximal to the distal tip and that broadens proximally to intersect the colony perimeter just proximal to the region of lateral out- flow. Most zooids in the stagnant area are senescent.

B. turbinata colonies are spiralled and consist of branches that typically are 2 zooids wide distal to bifurcations, grading to 4 zooids wide proximal to bifurcations. Water flow through colonies of B. turbinata (Fig. 6B) in still water is similar to that in B. turrita. Shape and behavior of expanded lophophores were not recorded.

Live colonies in flowing water. - Colonies of B. neritina were observed in ambient flow velocities of 0.25 cm to 15 cm per second. In ambient flow lower than about 1 cm per second, lophophores are undeformed and tend to pivot a few degrees to better intercept the current where possible. Lophophores oriented in the downcurrent direction generate a cylindrical sheath of water around their branches where the cilia-drived current causes net flow to be opposite the ambient flow. The external current flowing through the colony divides around downcurrent-facing branches as though there were an invisible shield at a distance

88 Frank K . McKinney and others

A

LETHAIA 19 (1986)

B

Fig. 6. 0 A. Percent zooids per whorl occupied by polypides in four colonies of Bugula furbinafa. 0 B. Diagrammatic longitudinal section of B. furbinafa showing distribution of polypides (stippled bars) and downward, obliquely centrifugal flow surrounding interior stagnant region.

about equal to branch diameter around their reverse side.

Lophophores in ambient velocities of 1 cm to about 5 cm per second are progressively more deformed from their bell shape as seen in still or more slowly moving water. The deformation is expressed as a broader or narrower flare, de- pending on orientation into, away from, or lateral to the ambient flow. The width of the region defended by cilia-generated currents on reverse sides of branches that face downcurrent diminishes with increased flow velocity and apparently disappears at about 5 cm per second ambient flow. Only the zooids that directly intercept the ambient flow receive its full velocity; those that are shielded by branches on the upcurrent side experience lower velocities and thus have differ- ent feeding behaviors and success.

At ambient flow up to 4 cm per second, lophophores are more active than in still water or at higher velocities. The higher activity includes more opening and closing and more tentacle flicking than in the other conditions. At these low ambient flow velocities, food particles can be seen to be caught across the entire colony, from

upcurrent to downcurrent sides. However, with increased ambient flow velocity, the area of par- ticle entrapment is progressively restricted toward the more protected, downcurrent side of the colony. At 4.5 cm per second ambient flow, lophophores in the middle and in the downcurrent areas are successful, at 10 cm per second only the most protected lophophores trap some particles from the turbulent water in the lee of the colony, and at 15 cm per second no feeding success is perceptible. Even at 15 cm per second ambient flow, tentacles are not withdrawn, but are drawn out downcurrent in narrow cones or are locally thrashed about in turbulent water.

At all velocities of ambient flow at which colonies or parts of colonies can feed, water and particles that are drawn through the successfully feeding lophophores pass directly towards and then past the branches from which the lophophores are protruded. A search was made for ex- amples of flow of filtered water along branches and for food-bearing currents passing from the reverse sides of branches through expanded lophophores, but none were seen.


and is virtually identical with that seen in B. turrita colonies (Fig. 5A).

Distribution of polypide-bearing zooids in Bugula turbinata resembles that in B. turrita and B. plumosa in constituting a hollow conical region whose apex corresponds with the apex of the colony. However, several generations of polypides regenerate in zooids of B. turbinata (Fig. 7 ) , whereas B. turrita and B. plumosa apparently

Polypide distribution in spiralled Bugula Tufts of Bugula turrita shed proximal branch systems as they grow, so that each consists of only the distalmost several whorls, typically about eight. The proximal, stolon-like section from which branches have been shed may be up to twice the length of the existing distal tuft by the end of the growing season. Within the several ranks of whorls of a tuft, feeding polypides occupy almost all autozooids in the distalmost four whorls (Fig. 5), which constitute the region of distal taper and active branch growth. Beginning near the distal tip of the tuft, a proximally expanding zone, centered on the colony axis, consists of senesced zooids that lack polypides (Fig. 5). The senesced zone is surrounded by a conical zone of functioning, polypide-bearing zooids at branch tips. The senesced zone eventually ex- tends out to branch tips in the seventh or eighth whorl, and it is at that point that dead branch systems tend to be lost from the colony.

The zone of stagnant water in the interior of B. turrita colonies corresponds to the zone of senesced zooids. Percent zooids senesced within a whorl gives a low estimate of the relative width of the axial senesced zone, because of exponential increase in total length of the zooid-bearing branches away from colony centers as branches divide and increase in number. For example, in the sixth whorl, the axial senesced zone may in- clude only 40% of the zooids but occupies about 65% of the diameter of the whorl. The relationship between radius of senesced area and number of zooids senesced within B. turrita is similar to the relationship in adeoniform bryozoans between proximal length of branches in which zooids are closed by calcification versus branch area actually occupied by such zooids (Cheetham & Hayek 1983).

Colonies of Bugula plumosa from off Gill- stone, Scilly Isles, Great Britain, are more tightly coiled than those of B. turrita, because of a smaller angle between branch whorls and the colony axis, and either two or three branch systems constitute each whorl rather than regularly three as in B. turrita. However, as in B. turrita, polypide-bearing zooids are confined to a hollow conical region whose apex is centered on the distal tip of the tuft. In a single dissected colony, almost all zooids in the distal four whorls are occupied by polypides, and a proximally expanding axial senesced zone begins with the fifth whorl

Fig 7. Single branch system dissected from a colony of Bugufu /urbinu/u from Brcst. Brittany. France. Ill-defined bands of polypide-bearing zooids (patterned) alternate with thin bands of zooids in the polypide-degenerated stage (clear); only the most proximal zooids are permanently senescent. Note proximal increasc in brown bodies (black dots) per zooid from branch tips to senesced zone. Bar scale indicates approximately 1 mm.


have only one polypide generation per zooid. The degeneration-regeneration cycles in B. turbinatu result in thin, poorly defined bands of unoc- cupied zooids within the conical region where polypides occur, and distribution of polypides is less regular within and between colonies than in B. turritu. (Compare Figs. 5A and 6A.) Residual bodies, including a single bacterial cyst (Lutaud 1969) and brown bodies, accumulate within the zooids as is commonly seen in cyclostomes and also occurs in the cheilostome Steginoporellu (Palumbi & Jackson 1983). The number of brown

Figs. 5, 6 and 8.) In addition, distribution of mud-filled zooecia in Archimedes is less regular than polypide-bearing zooids in the two species of Bugulu, being more variable between whorls and differing more pronouncedly between colonies, However, the moving average of proportion of mud-filled zooecia in adjacent whorls in all colonies clearly demonstrates the proximal de- crease in occurrence (Fig. 8). There is a corre- sponding proximal increase in average thickness of terminal diaphragms that cap spar-filled zooecia.

bodies per zooid increases proximally (i.e. toward the colony axis) in each branch, which is simply a reflection of the greater age and therefore more polypide generation-degeneration cycles that have occurred in more proximal parts of branches. Up to six polypides successively occur in zooids at branch bifurcations, up to four polypides successively occur in other zooids within branches, and only one or two polypides occur in the elongate zooids along the colony axis before each of the zooids finally ceases functioning as a feeding member of the colony and becomes in- corporated in the expanding proximal senesced zone.

Occurrence of mud-filled zooecia in Archimedes Mud-filled zooecia in Archimedes zoaria are con- centrated in distal ends of distal whorls of branches (Fig. 8), as in spiralled Bugula. Proportion of mud-filled zooecia is much less in the distalmost 3 or 4 whorls than is that of polypide-bearing zooids in B. turritu, and it is some- what less than that in B. turbinutu. (Compare

Discussion The majority of modern erect stenolaemate bryozoans grow in cold marine environments that are relatively inaccessible or inconvenient for study of living colonies. As a result, colony flow is known for only a few erect, arborescent, unilaminate stenolaemates, all of which belong to Crisiu or Filicrisiu (Winston 1978, 1979). Lophophores in these species are delicate (<300 pm diameter), and, as in all stenolaemates thus far observed, lophophore bases are not protruded beyond skeletal apertures. Consequently, cilia-generated flow in colonies of Crisia and Fificrisiu is weak in comparison with that in colonies of Bugulu, but the pattern is the same (Winston 1978, 1979; per- sonal observation, F.K.M.). Similar colony forms and ranges of branch widths in living and fossil erect, arborescent, unilaminate stenolaemates and cheilostomes (McKinney, submitted), and similar cilia-generated flow patterns where known, suggest to us that it is more reasonable to infer flow patterns for the extinct stenolaemate Archimedes based on observation of the living

Whorl number

Fig. 8. Percent zooecia per whorl that are partially or completely filled by mud in what appear to be four nearly complete colonies of Archimedes intermedius (Ulrich) from the lower calcareous shale of the Bangor Limestone, Fox Trap, Colbert County, Alabama. Heavy line plots moving average of five whorls for all four colonies.

LETHAIA 19 (1986)

spiralled species of the cheilostome Bugulu than to depend on observation of living arborescent unilaminate stenolaemates, none of which are known to us to be spiralled.

Although branches and whole colonies of Bug- ulu are flexible, they are essentially immobile in still and gentle ambient flow. Therefore, under the quiet water conditions in which we observed spiralled Bugulu colonies, they mimic Archi- medes colonies in absence of bending of branches or colonies. The surface texture of Archimedes skeletons consists of numerous small nodes at ends of skeletal styles that extend above the in- tervening areas of lamellar skeleton. This con- trasts with the smoother cuticular surface of Bug- ulu. However, calcareous skeletons of living stenolaemates are invested in cuticle, which in double-walled species is separated by fluid and thin epithelial tissues from the skeleton and tends to present a smoother exterior surface than would the bare skeleton. Archimedes was double-walled, so would have had a surface texture more similar to that of Bugulu than the bare skeleton suggests. Any hydrodynamic differences between branches of Archimedes and Bugulu are presumed not to significantly affect comparison of the overall flow patterns within the colonies.

Observations on living colonies of Bugulu reported here support and extend those reported previously. Passage of cilia-generated flow from frontal sides to reverse sides of branches was observed by Cook (1977) and by Winston (1978, 1979). Cook (1977) also noted that functioning polypides in B. turritu are to be found in distal portions of branches. Okamura (1985) demon- strated that feeding success is progressively restricted to more downcurrent portions of colonies of B. stoloniferu with increased ambient flow velocity.

Spiralled colonies of Bugulu have been hypothesized to bend downcurrent in flow and to feed from the quieter, turbulent water in the distal lee of colonies (Warner 1977). Although this hypothesis is consistent with distal concentration of polypide-bearing zooids, no laboratory or field studies of feeding in ambient flow have been published for living spiralled colonies.

Cilia-generated flow has been observed for over 30 species of bryozoans with erect, arborescent, unilaminate colonies (Cook 1977; Win- ston 1978, 1979; this paper). In all instances, water is drawn towards lophophores from the region above the bell, through tentacles and then past the lophophore-bearing branches to the reverse

Flow and polypide distribution in BUGULA 91

sides. To hypothesize any other direction of movement, such as from reverse to frontal or parallel with branches, for self-induced flow in fossil arborescent, unilaminate colonies of cheilostome or stenolaemate bryozoans is not sup- ported by any known living representative of the phylum. For inference of colony-wide flow in Ar- chimedes colonies we therefore assume that frontally placed lophophores, whether oriented normal to branches or inclined some degree distally, drew water to be filtered from above frontal sides of branches and forced filtered water through fenestrules to the reverse sides of branches.

Polypide recycling by degeneration and regeneration is widespread in cheilostomes (e.g. Stach 1938; Dyrynda & Ryland 1982; Palumbi & Jack- son 1983), including Bugulu (e.g. Romer 1906; Correa 1948; Dyrynda & King 1982), and in stenolaemates (e.g. Borg 1933; Boardman 1971, 1983). Although uncommon (Dyrynda 1981; Dy- rynda & King 1982), absence of polypide recycling is known for some species of Bugula (e.g. Nielsen 1981; Dyrynda & King 1982).

Essentially continuous distribution of polypides in distal branches of colonies of Bugulu turritu versus presence of interspersed regressed zooids and proximal accumulation of brown bodies in distal branches of B. turbinatu probably reflects absence of polypide recycling and more ephemeral existence in the former and presence of polypide recycling and more persistent existence in the latter. Similar correspondence between colony persistence and polypide recycling has been documented in the cheilostomes Chur- tellu pupyruceu (larger number of recycled generations, more persistent) and B. j7ubellutu (smaller number of recycled generations, more ephemeral) (Dyrynda & Ryland 1982). These observations on differences in polypide distributions and investment in persistence suggest that the more heavily calcified, apparently more persistent colonies of Archimedes, probably had polypide recycling and distribution of functioning zooids that more closely resembled that of B. turbinutu than that of B. turritu. This conclusion is sup- ported by observation of interspersed mud-filled and spar-filled zooecia in distal whorls of Archi- medes, presuming that at least some spar-filled zooecia represent regressed zooids and mud- filled zooids represent polypide-bearing zooids.

A ciliary filter-feeding organism typically is de- signed such that food-bearing and filtered water are separated, with minimal effort expended in

92 Frank K. McKinney and others

refiltering water that it has depleted of nutrients (by inference from description of filter-feeding in diverse invertebrates in Jorgensen 1966). How- ever, in still water the serpulid polychaete Spi- robranchus giganteus giganteus, which bears a spiral whorl of ciliated tentacles, generates a flow that is incurrent from below the tentacle crown, that passes through several whorls, and that is excurrent above the crown (Strathmann, Cameron & Strathmann 1984). On exposed reefs where the species naturally occurs, vigorous wave surges probably prevent substantial refiltering, whereas some does occur during slacks. Similar conditions probably attain for spiralled Bugula species, which filter water through several levels in still water but live in subtidal to cryptic lowest intertidal zones where moderate to gentle wave and current action undoubtedly cause some differences in flow through colonies from that observed in still water, as was seen to be the case for B. neritina and B. stolonifera.

Previous hypotheses of water flow through Ar- chimedes have assumed that water is filtered only once. However, in spiralled colonies of Bugula, which are the best modern analogue of Archi- medes’ colony form, cilia-generated flow in still water passes through several whorls where functioning polypides occur at distal ends of colonies, before exiting the colony laterally. Large num- bers of Archimedes occur in fine-grained lithol- ogies that were deposited in quiet waters in the lee of shoals and in other protected or quiet bot- toms (McKinney 1979; McKinney & Gault 1980). Ambient flow near the bottom in such areas was probably so low that cilia-generated colonial wa- tar flow patterns were little affected by it.

Archimedes colonies grew upright, away from the substratum. Common occurrence of secondary spirals and virtual absence of indications of ancestrular origins suggest that colony toppling and growth of new colonies upward from margins of distal whorls was an important part of the life cycle (McKinney 1983). If distribution of functioning polypides were known for the erect colonies, patterns of water flow could be reasonably inferred by comparison with flow through spiralled Bugula.

Distribution of mud-filled zooecia in well-preserved Archimedes suggests the possible general distribution of functioning polypides at the time that colonies fell. However, there are two possible post-toppling modifications that could cause eventually mud-filled zooecia to not correspond precisely with polypide-bearing zooids at the

LETHAIA 19 (1986)

time that a colony fell. (1) Production of secondary spirals from margins of some distal whorls indicates vitality of prostrate colonies for some time after falling. During this time, some previously functioning zooids could be closed by thinly calcified terminal diaphragms, particularly in the distal whorls where presence of secondary spirals indicates that skeleton could be actively secreted after the colony fell. (2) Stresses placed on branches, either while the colony lies on the substratum, or after burial and during compaction of the surrounding mud, may have cracked terminal diaphragms and allowed infiltration of mud into zooecial chambers that had been capped by terminal diaphragms much earlier than the time when the colony fell. We infer that the former may have produced fairly extensive reduction in the representation of polypide-bearing zooecia in distal whorls. Observation of only a few ruptured diaphragms suggests that the latter has resulted in generation of relatively few mud-filled zooecia. We therefore interpret the curve that plots the moving average in Fig. 8 to under-represent by an unknown amount, the percentage of polypide-bearing zooids near the ends of branches in the distal few whorls but to be a fair representation of them for the more proximal. Functioning polypides in typical Archimedes likely were dis- tributed much as in B. turbinata (Fig. 6) , that is, present in most but not all zooids in the most distal whorls and progressively more restricted to branch tips proximal to a point where no more occur.

Flow of nutrient-bearing water through Archi- medes colonies in which whorl separation is only a few mm, as in spiralled colonies of Bugula, is therefore hypothesized to have been incurrent from the distal end of the tapered colonies. Flow was downward and slightly outward through a few whorls of functioning zooids, and filtered water eventually was excurrent proximal to the polypide-bearing zooids. We have not examined loosely coiled Archimedes species such as A . laxus in which whorls are separated by over 10 mm and in which there may have been in-and-out flow between successive whorls as hypothesized by Cowen & Rider (1972). However, flow through spiralled Bugula in which whorl separation is similar seems to be the best basis for inferring the flow patterns in the majority of Archi- medes species and specimens in which whorls are separated by about 5 mm or less. Acknowledgments. - Some of the specimens of Bugula turrita. B. turbinata. B. plumosa. and Archimedes intermedius, were

LETHAIA 19 (1986) Flow and polypide distribution in BUGULA 93

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provided by T. J . M. Schopf (deceased), G. Lutaud, P. Hay- ward, and J . Waters, respectively, and are much appreciated. The University of North Carolina’s Institute of Marine Sciences provided space for our use when we examined live colonies of B. neritina and B. stolonifera. We thank R. L. Anstey, J . Bishop. J. Chimonides, P. L. Cook and J . B. C. Jackson, who read the manuscript. The drafted figures were produced by M. J . McKinney. Appalachian State University provided support through a University Research Grant. Acknowledgment is made to the Donors of the Petroleum Research Fund, admin- istered by the American Chemical Society, for support of this research.

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flow and polypide distribution in the cheilostome bryozoan bugula and their inference in archimedes

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