Table Of ContentReference: Biol. Bull 183: 27X-296. (October. 1992)
Characteristics of Carbonates of Gorgonian Axes
(Coelenterata, Octocorallia)
J. C. LEWIS, T. F. BARNOWSKI, AND G. J. TELESNICKI
Department ofBiological Sciences, Brock University. Si. Catharines, Ontario, Canada L2S 3A1
Abstract. Axial skeletons of 13 species of gorgonians The mechanical propertiesoftheaxiscan vary(Jeyasuria
wereexamined bySEM, X-raydiffraction, and polarizing and Lewis, 1987) with the sclerotization ofthe gorgonin
microscopy. Calcite, though occasionally amorphous is (Goldberg, 1976)andcalcification (KingsleyandWatabe,
the majorbiogenic carbonate ofaxes. Non-biogenic min- 1987). Usuallythemajorcomponent oftheaxial skeleton
eralization maybecalcitic, amorphous, oraragonitic. Axes is the gorgonin, composed mainly ofcollagen fibers in a
ofPlexaurellacontain numerous, lenticular, calcitic loculi proteinaceous matrix(Leversee, 1969). Theprotein matrix
ofspherulitic prismaticcrystals. Mineralization in Ellisella is largely uncharacterized, but the collagen, though mod-
barbadensis is in the form ofconcentric layersofperpen- ified (Goldberg, 1973, 1976; Wainwright el ai, 1982), is
dicularly oriented, lath-shaped crystals that extend characterized as collagen.
through the annulations. Numerous longitudinally ori- Gorgonin isdepositedextracellularly in concentriclay-
ented collagen fibers perforate the crystals. Mineralization ersaroundacentral, hollow, chambered canal thatseldom
in Lophogorgia cardinalis is in the form of crescentic, exceeds 100 ^m in diameter. Goldberg's (1973) micro-
shield-shaped, flat, laminated plates composed of alter- graphs of fractured surfaces show that these layers are
nating layers ofcalcified (sheathed) and uncalcified col- made of collagen fibers. The fibers appear to be lath-
lagen fibers. The fibrous component in all species is ori- shaped not round asis mammalian tendon (Weise, 1988).
ented parallel to the longitudinal axis ofaxes. Fine striae The three-dimensional fibrous texture of gorgonin is
ontransversely fracturedcrystalsofspeciesofPlexaurella complex, but shows a preferred axial orientation (Gold-
and E. barbadensis probably represent daily growth berg, 1973). The axis is thus flexible (when wet) and has
banding. The functional associations of mineral forms a high tensile strength. The mechanical properties ofcol-
with stiffness, resistance to twist, and water movement lagens vary widely. Different chemical and macromolec-
zones are discussed. ular composition as well as the organization ofcollagen
fibers (Goldberg. 1976), profoundly influence their me-
Introduction chanical properties.
Though flexibility can apparently be controlled or
The gross morphology of a gorgonian colony is pri- modulated by sclerotization of the collagen within the
marily the product ofits variably branching axial skeleton axial skeleton, a widely used method ofstiffening axes in
(Muzik and Wainwright, 1977), which is composed pri- gorgonians isextracellulardeposition ofcarbonates within
marily ofa collagenous matrix called gorgonin (Barnes, the collagen interstitial spaces (Lowenstam, 1964; Jeya-
1980; Goldberg, 1976). The function ofthe axis as a me- suria and Lewis, 1987). Jeyasuria and Lewis (1987) de-
chanical support system isbased on octocorals beingpas- termined the Young's modulus ofthe axial skeletons of
sive suspension feeders that collect particulate food from thirteen species of holaxonian octocorals representing
flowing water. The axis must be rigid enough to hold the twelvegenera and foundthat theyrange from 0.2 Gdynes/
fragile polyps off the substratum and must be able to cm2 to 90Gdynes/cm: axial stiffness also correlated well
:
withstand thetotal watervelocities forthe particular hab- withzone-relatedwatermovement. Relativequantitiesof
itat or zone inhabited (Muzik and Wainwright, 1977). calcareous material in the axial skeletons were strongly
correlatedwith Young'smodulus, suggestingan important
Received 16 August 1991; accepted 1 July 1992. role forcalcareous material in modulating the mechanical
278
GORGONIAN AXIS CARBONATES 279
properties ofthe axial skeleton. Modulation ofaxial stiff- intra- and interspecific comparisons ofcollagen fiberori-
ness through calcification would be an effective mecha- entation, calcified loculus orientation, and mineral crys-
nism for dealing with the different hydrodynamic forces tallographic form withintheaxis, andtodescribe indetail
encountered at various depths. the calcified aggregates in several species.
The two majorcalcium salts used in skeletal structures
arecalcium phosphates and calcium carbonates. Usually, Materials and Methods
phosphates occur in conjunction with collagen, and car-
bonates in conjunction with glycoproteins. Phosphates The specimens ofoctocorals used for this study were
tendtobethemajorform in vertebratesand brachiopods; obtained during field trips to the reefs ofTobago, West
carbonates in most other invertebrates (Vincent, 1981) Indies. Most of the samples were collected from the
including gorgonians. Jeyasuria and Lewis (1987) com- northeastern tip of the island between 1984 and 1988.
pared the mole percent MgCO3 in Mg/Ca(CO,) ofthirteen The 13 species used were chosen from ten genera so as
species ofoctocorals. Three distinct groups were found: to representabroadarray ofoctocorallian morphological
14-18 molepercent MgCO,, 33-42 molepercent MgCO,. and compositional characteristics. Whole colonies were
and 71-85 mole percent MgCO?. X-ray diffraction pat- collected intact, dipped in \(Y"o formalin, air dried, and
terns for E. barbadensis, from the first group, showed transported to Brock University for dry storage.
high magnesium calcite as the crystallographic form of Species were identified with the aid ofBayer's (1961)
thecarbonate mineral. The higherpercentages are chem- guide"TheShallow WaterOctocoralliaoftheWest Indian
ically indicative ofdolomite and magnesite respectively, Region". They are all in the phylum Cnidaria. class An-
but crystallographic mineral type was not determined by thozoa. subclass Octocorallia. order Gorgonacea, and
X-ray diffraction. The substitution ofsmaller ions such suborder Holaxonia. Those in the family Plexauridae in-
as magnesium, carrying the same charge as calcium into clude the species Plcxaitrajlexuosa. Plexawella grisea,
a calcium carbonate matrix, increases the density ofthe Plexaurella fiisijera. Plexawella nutans. Eunicea iniir-
ionic packing. This results in both higher densities and nejorti. Pseudople.xaura porosa, and Muricea nuiricata:
greater hardness (Vincent, 1981). andinthe familyGorgonidaearethespeciesLophogorgia
The process ofbiomineralization can be biogenic and cardinalis, Gorgonia rcnialinu. Leptogorgia virgulata,
mediated by the organic matrix, in which case the pre- Pseudopterogorgiaacerosa, andPseudopterogorgiabipin-
cipitation process is controlled by a biological system, or niita: and in the family Ellisellidae is the species Ellise/la
it can be nonbiogenic and simply biologically induced, barbadensis.
but not controlled. The calcified loculi evident in some Cortex and adherent material were removed and the
species ofoctocorals are the result ofa biogenic process axisexposed. Sections were then cut from the axis, either
(Wainwright. 1988). Crystal formation by organisms is with ajeweler's saw ora fine-toothed, circular. Drommel
commonly controlled by an array ofextracellular proteins blade. Samples meant to show cross-sectional and lon-
and polysaccharides. In skeletal mineralization, these gitudinal surfaces were taken from bases, mid-sections,
macromolecules generally form a mold or framework in and tips ofeach colony. Three series were cut. The first
which the crystals grow. The macromolecules on the sur- set was dipped in a sodium hypochlorite solution, which
face ofthis organic matrix are most directly involved in dissolved the organic matrix and exposed calcified inclu-
regulating crystal nucleation and growth (Addadi el ai. sions. Thesecondserieswasetchedin 12%trichloroacetic
1987). The polysaccharides are generally sulfated and acid, dissolving the calcified aggregates. The third series
carboxylated (Weiner el ai. 1983). The type of mineral ofsampleswerebuffed with an emery board. Each species
nucleated may reflect the molecular structure ofthe nu- was then examined under dissecting and compound mi-
cleation site. Weiner cl ai 1983) have proposed that the croscopes.
(
mineralcrystal form(/>., calciteoraragonite)isdependent Measurements on those samples containing substantial
on the nucleation site. calcifiedaggregatesweremadewithanoptical micrometer.
In thisstudy, the morphology ofthe axial skeleton was The proportions oforganic matrix to calcified structure
examined in representatives often genera ofgorgonians. were derived from cross sections: the amount ofcalcified
The 12 specieschosen representan axial mineral gradient material wascomparedwith theamount oforganic matrix
inwhichthe valuecalcium + magnesium/dry weight var- along a series ofradial lines.
ies from 0.15-25'; (Esford and Lewis. 1990), and the Alizarin red S staining was also done to indicate the
mineral form based on atomic absorption spectroscopy extent ofmineralization. Samples were etched in bleach
could be aragonite. calcite. dolomite or magnesite (Jey- for up to 30 min, then washed in deionized water. They
asuria and Lewis. 1987; Esford and Lewis, 1990). Light were then placed in a vial with an Alizarin Red S stain
microscopy, polarizing microscopy, scanning electron for 7-10 min and rinsed with deionized water. This stain
microscopy, and X-ray diffraction were used to perform colors calcite and aragonite red. and dolomite blue. The
280 J. C. LEWIS ET AL.
procedure wasalsi i :hin translucent shavings cut (Polaron PS-3) for 60-120 s, and examined in a Hitachi
from unetched :\ a #10 scalpel blade. Shavings S-570 scanning electron microscope.
wereexamine*.] uht microscopeata magnification
of 1000X. Results
Small a -'s, about 1.5 cm\ were stripped of
all U' and immersed in sodium hypochlorite The gorgonian axes examined were morphologically
solution until all ofthe organic matterdissolved. The re- diverse. They ranged from axes that were white and
maining participate matter was then rinsed several times heavilycalcified, through those with white, crystalline ag-
with deionized water. The mineral was then filtered and gregates embedded in brown gorgonin, to those with no
collected on #1 Whatman filterpaper. With a mortarand apparent mineralization and with gorgonin that varied
pestle, the residual powder was ground to a fine consis- from brown and fibroustoalmostglassy black. Dried axes
tency. A Picker 2087 generatorwas used to diffract an X- exhibit some artifacts due to dehydration. There is often
ray beam through the powder, which had been affixed to some longitudinal checking or cracking ofthe gorgonin,
aglass plate with silicon vacuum gel. A graphical readout but it is usually not severe. Heavily mineralized axes ex-
representingthetaangleswasproduced. Diffraction peaks hibit theleast artifactual splitting. Axeswithwhatappears
were then compared to standards so that the mineralized to be amorphous, dense gorgonin show moderate check-
crystal lattice ofeach ofthe samples could be identified. ing. Axesthat are readily distinguishableasfibrous usually
No diffraction pattern wasgenerated from some ofthe show the greatest degree ofartifactual splitting. Measure-
samples. Powder from these samples was packed into a ments taken with calipers revealed no significant differ-
mm
0.03 capillary tube, and an X-ray beam was passed ences in axis diameter between fresh, dehydrated, and
through thespecimen usingaNoniusCAD-4automated, rehydrated samples. The 12 species examined can be
single crystal X-ray diffractometer. The X-ray beams are readily separated into 3 groups on the basis ofmineral-
diffracted directly on to a film plate as diffraction rings. ization.
From the spacing between rings, the theta angles were Species with high Ca + Mg values (i.e., 10-25% Ca
calculated for comparison to known mineral standards. + Mg/dry wt; Jeyasuria and Lewis, 1987; Esford and
Lewis, 1990) contain easily distinguishable calcified ag-
Scanning electron microscopy (SEM) gregates. The species making up this group include Elli-
Various preparative techniqueswere utilized toexpose se/ln harhiulcnsis, Plexciurel/a nutans, Plexawellagrisea,
the outer, inner, lateral, longitudinally fractured, and the and Plexaurellafusifcra. With the exception of E. har-
transversely fractured surfacesoftheaxial skeleton. Frac- badensis, the mineralized loculi in cross-sectional aspect
tured transverse surfaces were obtained with a fine hand- are semi-lunate and oriented so their concave surfaces
saw, or by bending or twisting the axial skeleton perpen- face the central core ofthe axis. In longitudinal aspect,
dicular to the longitudinal axis until it fractured. Longi- loculi are lenticular in shape. The number ofloculi per
tudinal surfaces were exposed by splitting cross-sectional unit area is greatest near the central region of the axis.
specimens with a scalpel blade. The fractured specimens Individuals ofE. harhmlensis have a mineralized central
were examined untreated or after further treatment. To rod surrounded by mineralized cylinders reminiscent of
remove the gorgonin and collagen fibres and to expose a single bone osteon. As with the species ofPlexawella.
the calcareous matrix, specimens were treated with con- the proportion ofcalcified material to organic matrix de-
centrated hypochlorite bleach (Chlorox or Javex) for creases distal to the axis center. The cylinders near the
various periods, from 30 s to 20 min, depending upon axial periphery deform into sickle-shaped aggregates.
theamounts oforganic matrix tobe removed. To expose The percentage of cross-sectional area occupied by
organic matrix and remove the calcareous components, mineralizedaggregatesvarieswithspeciesandlongitudinal
specimensweretreated with 10% HC1 or2%ascorbicacid. position along the axis. The approximate percentages of
To remove large amounts ofthe calcareous material rel- mineral aggregate are: E. barbadensis tip94%, mid-col-
atively rapidly orto freecollagen fibres from thegorgonin. ony 81%, base46%-; P. grisea tip 89%>, mid-colony63%,
concentrated HC1 was used for intervals ranging from a base29%;and P. nuians tip 85%, mid-colony 57%, base
fewminutestoseveral hours. When onlya relatively light 32%;andP.fmifera tip75%-, mid-colony 53%,base37%.
etching ofa fractured or exposed calcareous surface was In all cases, the proportion of gorgonin to mineral in-
desired, dilute 2% ascorbicacid was used forshort periods, creases toward the base.
30-240 s. Combinations of these treatments were also Those species with a moderate amount of Ca + Mg
used to determine relationships between calcareous and (i.e.. 2-10%.Ca + Mg/dry wt)(Jeyasuriaand Lewis, 1987;
organic matrices. Powder residue was also examined. and Esford and Lewis, 1990) include Leptogorgia virgu-
Specimens were mounted on aluminum SEM stubs laiii, Lophogorgia canlinalis, Pseudopterogorgia bipin-
with double-sided mounting tape, gold sputter-coated ncild. and Pseudopterogorgia ncerosn. These species
GORGONIAN AXIS CARBONATES 281
contain bundles ofrelatively large collagen fibers. Mineral Aliziran red staining of heavily calcified species, such
is associated with the fiber bundles ofPseudopterogorgia as Plexaurella fusifera. Plexaurella nittans. Plexaurella
bipinnata and Pseudopterogorgia acerosa (Fig. la). grisea. and Ellisella barbadensis, showed good differen-
Whether the collagen fibers themselves are mineralized, tiation. The high magnesium calcite loculi stained red,
or are encased by mineral, is not clear. Bleach etching and the interstitial matrix remained unstained (Table 1).
revealsthin, cylindrical, calcified sheetsbetween the layers The moderately calcified species, such asLeptogorgia vir-
oforganic matrix ofboth Leptogorgia virgulata and Lo- gulata. Lophogorgia cardinalis. Pseudopterogorgia bip-
phogorgia cardinalis. innata. Pseudopterogorgia acerosa, and Gorgonia vental-
In contrast, those octocoralswith Ca + Mgcontents of ina contain calcified, lath-like sheets rather than discrete
1-<0.1% Ca + Mg/dry wt (Jeyasuria and Lewis, 1987; loculi. They stained with less differentiation. It appears
Esford and Lewis, 1990) appear in cross-section to be that the mineral is contained within or around the col-
composed offibrousgorgonin. No mineral aggregatesare lagenous fibers, producing the impression ofwidespread
apparent. Included in this group are PlexauraJlexuosa, mineralization in low concentration. Axes of Plexaura
Mwiceamuricata, and Euniceatourneforti. Though Gor- Jlexuosa, Muricea muricata, and Eunicea tourneforti did
gonia ventalina has a Ca + Mg content within the mod- not stain with Aliziran red, an indication that no min-
erate range (2-10%) ofthe previous group, it is morpho- eralization occurs in these species. Powder, collected as a
logically similar to this group. Despite apparent lack of residue after the organic matrix was digested, yielded
mineralization, when all organic material is removed by crystalsfrom each species. All stained positively(red); but
hypochloritedigestion, a fine, crystalline residueremains. speciessuch as M. muricata and Eunicea tournefortipro-
Most ofthese are similar to crystals noted in the hollow duced limited amounts ofcrystal, little ofwhich stained.
coreofaxesonSEM examination. Crystalsseparated from Detailed scanning electron microscopic examination
the matrix are highly variable in shape (Fig. Ib, c, d). wasdoneon thecalcareouscomponentsofaxesofseveral
Individuals ofM. muricata exhibit crystals roughly sca- heavily mineralized species.
lenohedron in shape, an alternate habit orform ofcalcite
(Fig. Ib). In PlexauraJlexuosa (Fig. Ic) and many other Plexaurella nutans, P. grisea andP. fusifera
species, crystals with sharp edges and regular geodesic
forms characteristic of both nonbiogenic mineral depo- Becausethecarbonatedepositsin theaxesofthesethree
sition and calcite can be found. Some ofthe crystals in species showed only minor differences, they are treated
Eunicea tourneforti (Fig. Id) are needle-like and charac- as a single group.
teristic ofaragonite. Axial skeletons ofspecies ofPlexaurella are composed
In every species, the points oflight extinction asdeter- of fibrous gorgonin and calcareous loculi. In a bleach-
mined from polarizing microscopywithcrossed Nicholls' etched cross section ofan axis ofPlexaurella nutans. the
filters, indicateafibril orientation parallel tothelongaxes large number ofloculi and their tight packing are clearly
ofthe colony. The extent ofextinction was high, and the evident, and they form a substantial component of the
angles oflight extinction occurred at consistent angles of axis (Fig. 2a). Elongate loculi are semi-lunate, through
horizontal stage rotation at and 90. In crossed Nich- anvil, to kidney-shaped in cross section (Fig. 2b). Widths
olls' polarizing microscopy, polarizing filters are posi- vary from about 40 ^m to more than 250 /urn. Inner (to-
tioned above and below the specimen and are oriented at ward the hollow core), outerand lateral surfaces ofloculi
90 to each other. Parallel-oriented polarizing elements are morphologically distinct (Figs. 2b, c). Surfaces of
in the specimen will cause light extinction when aligned transversely fractured loculi exhibit fan-shaped, crystal
with the polarizing planes of either filter. These trends patterns that radiate peripherally (Figs. 2c. d). At high
were equally apparent in all species, and the interlocular magnification, after light ascorbic-acid etching, fine lateral
organic fibrillae ofthe heavily calcified samplesalsoshow striations that vary in width from 0.3-0.5 /im are visible
a distinct uniform orientation. in all three species (Fig. 2d).
The X-raydiffraction patternsindicate high magnesium Individual loculi are elongate, pallisade-shaped, lon-
calcite as the crystallographic mineral form in Plexaurella gitudinally oriented with respect to the axis, and occa-
fusifera, Plexaurella nuttins. Plexaurella grisea, Ellisella sionally branch (Fig. 3a). The outer surface ofa loculus
barbadensis, Pseiuli>pten>gorgia acerosa, Pseudoptero- is composed of the ends of the crystal plates (Fig. 3b),
gorgia bipinnala. and Mwicea muricata. Amorphous horizontally oriented and irregularly fusiform. Exposed
mineral, that which does not produce a clear diffraction ends ofcrystals appear as small, thin, narrow transverse
pattern, wasfound in Lophogorgia cardinalis. Leptogorgia plates that terminate at the outer surface ofthe loculus
virgulata, PlexauraJlexuosa. and Gorgonia ventalina. The (Fig. 3b). Localized groups of plates exhibit similar ori-
mineralfromEuniceatournefortirwasfoundtobearagonitic entationsslightlydifferent from adjacentgroups(Fig. 3b).
(Table I). The innersurfacesofloculi exhibit longitudinally oriented
282 J. C. LEWIS ET AL.
Figure 1. (a)Sim:, >| atihroidcrystalaggregatefromthematrixoftheaxisof/'.ttWrv"''''<',','"''.Whipintnila. Thestructuresbeartheimpressions
ofcollagenfiberlayersbetween whichtheyoccur. X-raydiffraction pattern indicatescalcite. 2000X. (b)Mineralaggregatefromthehollowaxialcore
Mm
of iien innnailti \-i.i\ diffraction pattern indicates calcite. Crystal forms are scalenohedral, an alternate calcite form characteristic of non-
biogenic deposition. I300x. (c) Calcareous crystals from the hollow axial core ofI'k'xuuia llcxuma ofgeodesic form indicative oftypical, non-
biogenic,calcitedeposition. X-raydiffraction pattern isamorphous. 3800 . (d) Mineralaggregatesfrom the hollowcoreofEuniivuloiirncjarli. The
needle-likecrystal form ischaractensticofnon-biogenicaragonitedeposition. X-raydiffraction pattern indicatesaragonite. 1200X.
GORGONIAN AXIS CARBONATES 283
Table I
Stainingproperties, compositional, andmorphologicalcharacteristicsofinvestigatedspeciesofoctocoralliansrelativeto watermovement zones
Species
284 J. C. LEWIS ET AL
.'1/,'nr.
11
iiiii"
;
p
-r-^'^T&SBK?^
Figure2. (a)Crosssectionofableach-etched(gorgonin removed)axisofPlexaurellaniilum. Notethehollowcoreand numerous,tightlypacked,
semi-lunatecalcareouslocuh. 25 .(b)Bleach-etched(gorgonin removed),transverselyfracturedloculiofPlexaurellamttanx. Inner,outer,andlateral
locular surfaces are apparent. Note radiating, fan-like pattern on both transversely and longitudinally fractured surfaces. 161K. (c) Bleach-etched
singleloculusot Plexaurellagrixcu. Notethe fibroid pattern on theinnerlocularsurface,thestacked, fusiform,crystal plateendsoftheouterlocular
surface,andtheradiatingfan pattern on thetransverselycleaved surface. 950X. (d) Lightlyascorbic-acidetched, transverselycleavedlocularsurface
ofPlexaurella lit\t/cru Note the line, vertical striaewith a periodicity ofabout0.3 /im that may represent episodiccarbonatedeposition. 4700X.
GORGONIAN AXIS CARBONATES 285
oriented crystals (Fig. 5d). There are usually a minimum collagen fiber content become evident. The axis consists
oftwo sublayers on each surface ofan annotation. ofnumerous, smooth concentric annular layers reminis-
centofasingleosteon frombone. Theprincipal individual
Lophogorgia cardinalis crystalline components of the annulations are elongate,
lath-shaped, perpendicularly oriented with respect to the
Numerous, crescentic, lamellar, calcareous plate loculi axis, and they extend across the entire width ofthe an-
are a major component of the axial skeleton (Fig. 6a). nulus. Whetherthese are singlecrystals or multiple crystal
Removal of gorgonin and collagen by bleach etching compositeswas not determined. These units, stacked like
eliminates the overlying support for the calcareous com- two-by-fours in a lumber yard, are highly resistant to
ponents ofthe loculi. Subsequent dehydration, necessary compressional forces, but like bricks in a wall held only
for examination in the SEM, introduces artifactual frac- by mortar, provide little resistance to tensional forces
tures in the platesand breaksthem into smaller, irregular which would tend to lift them apart. Tensional forcesare
blocks(Fig. 6b). Theshield-like loculiare irregularin out- accommodated by the numerous, high tensile strength,
lineand haveconnectionswith neighboringlocularplates uncalcified, collagen fibers (Moss, 1964) that perforate
(Fig. 6c). The outer surface oflocular plates is composed the laths. These longitudinally oriented fibers are sur-
offine-grained, generally longitudinally oriented crystals rounded by calcareous material and appeartightly incor-
oraggregates (Fig. 6d). The interlocular gorgonin contains porated into it. Individual collagen fibers extend through
longitudinally oriented, layered collagen fibers (Fig. 6e) a minimum ofseveral laths, ifnot theentire length ofthe
0.1-0.3 jum in diameter. annulus. They can be thought ofas analogous to the ef-
Viewed edge-on, the longitudinally fractured platesare fectively non-extendible, iron reinforcing rods in concrete
seen tobranch laterally in a pattern reminiscent ofcardiac that strengthen it in tension. This construction produces
muscle fibersand to form fused connectionswithadjacent the stiffest, shallow-water gorgonian axis (Jeyasuria and
plate loculi (Fig. 7a). The loculi are also laminated (Fig. Lewis, 1987; Esford and Lewis, 1990) that has been re-
7a, b) with alternating layers ofsmooth, fine, longitudi- corded to date. It also has a comparatively high torsion
nally oriented crystals, or aggregates, and gorgonin-col- modulus(Jeyasuriaand Lewis, 1987)despitethe flexibility
lagen (Fig. 7b). A transverse fracture ofa loculus clearly of the collagen fibers. That is probably a result of the
reveals the lamination (Fig. 7c). The centers of many manner in which the lath-like, crystal aggregates are
crystals are hollow (Fig. 7c). Acid etching, to remove the stacked, but this was not examined extensively.
carbonate, leaves the fused and melted ends ofthe dense The elongate, whip-like individuals ofEllisella barba-
gorgonin-collagen layers ofthe lamellar plate as readily densis generally occur well below wave base in areas of
apparent layers in Fig. 7d. current-generated watermovementonly. Forcesgenerated
Discussion by such currents are high (Roberts ct ai. 1975), and this
is one reason for the high stiffness ofthe axis. The other
Octocoral axes are composed of a limited number of is as follows. The majority ofshallow water gorgonians
structural elements. Principally they contain variable occur in the surge zone where wave action returns them
amounts offlexible collagen fibers, embedded in a pliant, through the upright position approximately every 12 s
proteinaceous matrix, and minerals thatexist in a variety (open ocean wave period). Below wave base, where Elli-
ofcrystal forms and aggregate shapes (Kingsley and Wa- sclla barbadensis occurs, currents can be anywhere from
tabe, 1984). These components are assembled in a sur- constant and unidirectional through intermittent and
prisingly large range of forms (Telesnicki, 1990; Bar- multidirectional. In most tidal locations, bidirectional
nowski. 1991), the functional significance of which is currentsalternatingabouttwiceperdaycouldbeexpected.
dimly known at present. Functional relationships can be In any case, the current iscomparatively constant for rel-
better understood ifstructure is known and can be used atively long periods (a few h). A comparatively stiffaxial
tocomplement, explain, and inferfunctional interaction. skeleton is required to maintain the polyps in a feeding
Detailed SEM examination of the carbonate inclusions position in the water column, and to keep the colony off
in three genera has revealed three substantively different the substratum under these conditions.
mineralization types from which some functional infer- Fine striae, approximately 0.3 fj.m in width, evident on
ences may be derived. cross sections lightly etched with ascorbic acid probably
represent episodiccarbonate accretion. Nodata have been
Ellisella
published on the rate ofelongation ofEllisella barbaden-
The axis of individuals of Ellisella barbadensis is ex- sis. let alone on the rate ofincrease in its diameter. The
tensively mineralized (about 30%/dry weight) by high striae could represent dailyaccretion rates; in which case,
magnesium calcite(Jeyasuriaand Lewis, 1987; Esford and the yearly increase in diameterwould be about 0.25 mm.
Lewis, 1990). Only when it is decalcified does the large Ifthey represented growth associated with different tidal
286 J. C. LEWIS ET AL.
Figure-V (a) Bleach-etched outerloculi ofPlexaurellatf/v.vcnareelongate,pallisade-shaped,longitudinally
oriented, occasionally branch, and fusewith otherloculi. Notein lowerleftcornerthespherical,crystalline
unitsthathavenotyetfusedcompletelyintoamatureloculus. 100 .(h) Bleach-etchedouterlocularsurface
iifr/i-\iinrc/lii ///w/m; composed ofouterendsofthe crystal plates. Most are fusiform. 4700 . (c) Bleach-
GORGONIAN AXIS CARBONATES 287
current regimes, ofwhich there would be about four per calcite of the high magnesium variety (Jeyasuria and
day, the increase in diameter would be approximately Lewis, 1987; Esford and Lewis, 1990). In these species,
1 mm/year. It could be that only currents from one di- crystallineaggregates(loculi), which arelenticularand fu-
mm
rection carry enough nutrient to permit carbonate de- siform, can be up to 5 in length and are semi-lunate
position, or that nocturnal currents do so. In those cases incrosssection. They areembedded longitudinally in the
there would be two striae per day deposited and an ac- gorgonin. As in all thegorgoniansexamined, thecollagen
cretion rate of0.5 mm/year. These are ahermatypic or- fibers course longitudinally through the proteinaceous
ganisms (Goldberg, 1973), therefore they are dependent matrix ofthegorgonin, butdonot penetratethecrystalline
on "captured" prey for nutrients. Other scenarios could aggregates. The loculi are solid, crystalline structures
also account forthe striae. Ifthediameter, includingthat composed ofregular, spherulitic. prismatic units similar
atthebase, accretesataconstant ratethatdoesnotchange to those ofmolluscan shell (Carter and Clark, 1985).
with age, then an individual with a basal thickness of 1 Species of Plexaurella occur in the surge zone where
cm (not uncommon) could be somewhere between 10 they are subjected to both wave and current-generated
and 40 years ofage. This is. ofcourse, a very crude esti- water movements that produce high forces in storm con-
mate. ditions. Normally, forces generated in the surge zone are
A series ofmicrographs ofrandomly taken specimens lowerthan thoseencounteredeitherin deeperwater(pro-
cannot be used to prove that dynamic processes occur in duced by current only), or in the shallower breaker zone
a particular sequence. Nevertheless, many micrographs (Roberts el at., 1975). In addition to the back and forth
ofannuli in various stages ofdevelopment have been ex- sway from wave action, there is also a twisting motion
amined, andwearenowconfidentthat annulusformation that is amplified by current. Species of Plexaurella are
canbeoutlined. Theformation ofanannularlayerbegins generally large (some up to 2 m in height) with compar-
withthedeposition offine, "seedcrystals" overthesmooth atively long, thick branches. The moderately high stiffness
outer surface of a previous, inner annulation. The fine and moderate torsion resistance ofthese species accom-
crystals initially have a random, granular appearance. As modate them to the forces in the surge zone. Separation
collagen fibers are synthesized and encapsulated within ofthe collagenousand mineral phases, with the retention
the fine seed crystals, the layer becomes longitudinally- ofapproximately similar proportions ofcarbonate (Jey-
striated with impressions ofthe collagen fibers. It is on asuria and Lewis, 1987; Esford and Lewis, 1990). may
the outersurface ofthis "seed-crystal" layer that the thin lowerthe stiffness from that ofEllisella barbadensis. The
perpendicularly oriented annulation crystals nucleate. lenticular crystalline loculi probably also stiffen the axis
Small, 'initial', annular crystals nucleate on the surfaces in the manner offiller particles (Koehl, 1982) and main-
ofthe fine crystals. Asthe fine annular crystals grow out- tain stiffness in a moderately high (forgorgonians) range.
ward, they becomeoriented perpendicularly by lateral in- The semi-lunate, cross-sectional shape ofthe loculi prob-
terference from adjacentcrystals. Thesefinecrystalsmerge ably allows species ofPlexaurella to rotate somewhat in
to form the larger, lath-shaped, perpendicularly oriented response to twisting forces and results in a moderately
crystal aggregates that span the annulus. Collagen fiber low torsion modulus (Jeyasuria and Lewis, 1987).
synthesis and deposition must occur prior to crystal Fine striae, about 0.4 ^m in width, evident on lightly
growth, since the longitudinally oriented collagen fibers
are incorporated within the crystalline material. When aasbcloyrrbeipcreasceindt-eetpcihseoddiccrocsasrbsoencattieonasccorfetloicounl.i,Noagadiantaphraovbe-
annularcrystalgrowth ceases, the skeletogeniccellsofthe been published on growth rates ofspecies ofPlexaurella,
axial epithelium secrete another layer of fine, capping
but theyappearto be very slowgrowing(circa 1 cm/year;
crystals.
Paul Yoshioka, pers. comm.). Ifthese striae are compa-
Genus Plexaurella rable to those from Ellisella barbadensis, and assuming
Axes of Plexaurella nutans. P. grisea and P. fusifera that one stria represents accretion overthe same time pe-
are extensively mineralized (about 20%/dry weight) by riod in both species (which may well not be the case).
etchedinnerlocularsurfaceofPlexaurellainilanswith longitudinalgroovesbetween finecrystals. Irregular,
rosette-likepatternsarethoughttorepresentnucleationsitesforspheruliticcrystalaggregatesoftheloculus.
2300x. (d)Surfaceofthelongitudinally-fracturedgorgonin layerbetween loculiofPlexaurellanutanswith
longitudinallyorientedcollagenfibres.Notethatthediametersofthecollagenfiberscorrespondtothegroove
diameters in 3c. 2300X. (e) Lightly ascorbic-acid etched, longitudinally fractured loculus ofPlexaurella
nutans. Several spherulitic crystal units are evident with crystal plates radiating fan-like from an inner
nucleation siteout tothe outeredge ofthe loculus. Note that some crystal plates branch and the seriesof
cavities where adjacent plates interfere with plate growth, \-ray diffraction pattern indicates crystalline
calcite. 3750X.
