AM. ZOOLOGIST, 9:1011-1020 (1969).
Comparative Calcibiocavitology: Summary and Conclusions
MELBOURNE R. CARRIKER AND EDMUND H. SMITH
Systematics-Ecology Program, Marine Biological Laboratory, Woods Hole,
Massachusetts 02543, and Pacific Marine Station, University of the Pacific,
Dillon Beach, California 94929
SCOPE
The magnitude of the broadly multidisciplinary problem of CaCO3-penetration
by organisms is impressively evident in the
papers of this Symposium. Although
many new findings are reported, the field is
mainly in the alpha phase of development
and there are conspicuous major voids in
our knowledge of the subject. Information
on known individual penetrating species is
grossly incomplete, and comparative biological aspects are just beginning to
emerge. The Symposium contains many
fine contributions, including noteworthy
papers on behavior, ultrastructure, physiology, and biochemistry. The degree of
ingenuity which both paleontologists and
neontologists have brought to bear on the
exploration of processes which take place
within an intractable, generally opaque,
crystalline medium, is admirable. If the
current activities of persons participating
in the Symposium portend the rate of continuing research, the field has a bright future.
DEFINITIONS
A primary consideration in the Symposial discussions at Dallas relative to penetration of hard CaCO-5-materials by organisms, was the interchangeable use of the
common terms "bore", "burrow", and
"drill", and "substratum" and "substrate",
and the meaning of "penetrate" and "exWe are grateful to J. M. Arnold, W. R. Cobb, H.
H. Chauncey, M. L. Jones, P. Person, A.
Smarsh, and R. T. Wilce for reading the
manuscript to this summary and for offering valuable suggestions. Preparation of the manuscript was
supported in part by U. S. Public Health Service
Research Grants DE 01870 and DE 2503 from the
National Institute o£ Dental Research. SystematicsEcology Program Contribution Xo. 190.
cavate". A lengthy disussion concerning
the use of these terms by the panel and
subsequent study lead us to recommend
the following standardization. No effort
has been made to standardize terminology
of the Symposial papers, as we believe this
will be done by writers themselves in future publications.
Penetrate: movement of an organism
(the penetrant), or one of its organs, into
a space (the penetration) hollowed out by
the penetrant in calcareous material.
The material may vary in consistency from
soft to hard, and enlargement of the space
may be accomplished by mechanical and
/or chemical removal. Resulting particles
may be pushed aside, voided to the exterior, or partly swallowed. The size of the
penetration may range from considerably
smaller than the penetrant to sufficiently
large enough to accommodate the whole
organism. The space may be used as a
passageway, for residence, protection, nutrition, or for other purposes. The concept
emphasizes passage of the organism, or a
part of it, into the material.
Excavate: removal of material by an organism (the excavator) to produce a cavity (the excavation). The term stresses
transfer of material, either by mechanical
or chemical means, and has the same
broad generic connotations as the word
"penetrate". Both words are useful, depending on the emphasis desired.
Substratum (pi., substrata): the material penetrated or excavated.
Substrate (pi., substrates): a specific
noun for the substratum when acted upon,
as by an enzyme.
Burrow (verb): excavation of a space by
a whole, or by part of an organism (the
burrower) in the substratum for the purpose of living its entire life cycle or a given
1011
1012
MELBOURNE R. CARRIKER AND EDMUND H. SMITH
interval of time within or on the substratum. The specific meaning conveyed is that
the whole organism, or part of its body,
resides within the excavated space (s). Burrowers may excavate a variety of substrata,
ranging from soft uncemented sediments
(Pelricola), to dense coral (certain bivalves), limestone (endolithic algae), and
molluscan shell (Penitella). The method
of burrowing may consist of pushing aside
loose particles, scraping out hard material
mechanically, chemical dissolution of the
material, or a combination of these. Rate
of burrowing is relatively slow, and the size
of the enlarging burrow is usually just
sufficient to accommodate the growing burrower.
Bore (verb): excavation of a hole (the
borehole) in the calcareous exoskeleton of
prey by a predator (the borer) by means
of one or more of its organs for the purpose of obtaining food (Urosalpinx and
Purpura), or injecting a substance into the
prey (Argobuccinum and Octopus) to facilitate entry into it. The rate of boring is
relatively rapid, and many boreholes are
excavated in numerous prey by an individual borer during its lifetime. This is in
contrast to burrowers where an individual
in its lifetime generally excavates only one
burrow or a single series of burrows.
The major functional difference between burrowers and borers is the the
former make excavations frequently larger
than themselves and take up residence in
or over them, whereas the latter produce
perforations always considerably smaller
than themselves for trophic purposes. The
morphology and size of excavations are
useful in the identification of many taxa of
penetrants (this Symposium; Carriker and
Yochelson, 1968), and these features often
also aid in distinguishing burrowers from
borers. The physiological types of penetrating mechanisms likewise may be diagnostic and may contribute to the separation of
burrowers from borers, but due to the
current paucity of information about these
processes in the various phyla, little can
be said about them at this time.
Bivalves which excavate burrows in
limestone, shell, and wood, and gribbles
(Limnoria) which hollow out burrows in
wood are commonly called "borers" in the
literature (Clapp and Kenk, 1963; Turner,
1966). According to the classification recommended here, however, the appropriate
term for these organisms is "burrowers",
and the method of penetration, "burrowing". Predatory, shell-boring, muricid
gastropods are known colloquially as
"drills" (Webster, 1965, p. 254); we recommend that the term be restricted to this
colloquial usage.
No term exists for the multidisciplinary
science dealing with the mechanisms and
products of excavation of dense calcareous
substrata by the wide range of plants and
animals discussed in this Symposium. This
is probably a reflection of the relative recency of experimental work in the field.
The term "caries" (L., rottenness), defined
as a progressive destruction of bone or
tooth, is well established in vertebrate biology; this word, however, is restricted in
meaning, and like the destruction of coral
by bacteria described in this Symposium
(DiSalvo) implies pathology. In view of
this deficiency, we have coined the following terms for consideration by future investigators. Cariogenic microorganisms are
included in the definitions.
Calcibiocavitology (calcib'iocavitol'ogy):
the science dealing with the hollowing
out of spaces in hard calcareous substrata
by organisms (L. calx, lime, calcium, calcium salts; Gr. bios, mode of life; L. cavus,
a space hollowed out; Gr. logos, branch of
knowledge, science).
Calcibiocavite: an organism (calciphytocavite, plant; calcizoocavite, animal) which
hollows out a space (burrow, borehole,
caries) in hard calcareous substrata.
Calcibiocavicole: an organism inhabiting
a space excavated by itself in a hard calcareous substratum; calcicavicole: an organism inhabiting a space excavated by another organism or by nonbiogenic forces in
a hard calcareous substratum.
CLASSIFICATION AND DISTRIBUTION
The calcibiocavites treated in this Sym-
TABLE 1. Classification of calcibiocavilics treated in this Symposiu
Type of
excavator
Type of
excavation
Bacteria
burrower
glomerate coral
chemical
Fungi
burrower
burrower
calcareous skeletons
and tube linings
beach rock
chemical
Algae
burrow
(caries?)
burrow
(caries?)
burrow
A Igae: Cya noph yceac:
Hormatonema paulocellulare
Hyella caespitosa
Algae: Phaeopliyccae:
Fucus vesiculosus
Invertebrala: various
Invertebrata: various
burrower
burrow
crystals of Iceland
spar
chemical
burrower
burrow
burrower
burrower
burrow
burrow
Porifera: Cliona celeta
burrower
burrow
Bryozoa
burrower
burrow
Sipunculoidea
burrower
burrow
cirriped and molluscan
shell; calcareous rock
calcareous rock
shell of bivalve,
Placopecten
Iceland spar and
bivalve shell
calcareous exoskeletons and rock
calcareous rock
Penetrant
Nature of
substratum
Purpose of
excavation
Mechanism of
penetration
Authors (this
Symposium)
nutrition?,
residence?
nutrition?,
residence?
nutrition?,
residence?
nutrition?,
residence?
DiSalvo
chemical
anchorage, other?
Barnes, el al.
}
residence, other?
residence, other?
Warme, ct al.
Evans
mainly chemical;
some mechanical
chemical mechanical?
chemicalmechanical?
residence, other?
Cobb
,'E
residence, other?
Soule, et al.
n
>
n
residence, other?
Rice
?
?
Cameron
o>
<;
?
residence, other?
Blake
o
mainly chemical;
some mechanical
residence, other?
Haiglcr
8
?
residence, other?
Jones
?
p
Scilacher
chemicalmechanical?
residence, other?
Tomlinson
?
?
Macarovici
mechanicalchemomcchanical?
mainly chemical;
some mechanical
residence, other?
Ansell, et al.
residence, sexual
maturation
Smith
chemical
Kohlmeyer
Craig, el al.
Golubic
o
Annelida: fossil
burrower
burrow
Annelida: Polychacta:
Polydora
Annelida: Polychaeta:
Polydora websteri
Annelida: Polychaeta:
Caobangia billeti
Crustacea: Cirripedia:
barnacles, fossil
Crustacea: Cirripedia:
barnacles
Mollusca: Bivalvia:
fossil
Mollusca: Bivalvia
burrower
burrow
burrower
burrow
burrower
burrow
burrower
burrow
burrower
burrow
burrower
burrow
burrower
burrow
Mollusca: Bivalvia:
Penitella conradi
burrower
burrow
calcareous exoskeletons
molluscan shells
molluscan shell;
Iceland spar
molluscan shell
calcareous skeletons
and rock
calcareous skeletons
and rock
calcareous skeletons
and lock
calcareous skeletons
and soft to hard rock
abalone shell
:>
O
'*
H
[-1
2
0
o
TABLE 1 (continued).
Penetrant
Mollusca: Bivalvia
and Gastropoda
Mollusca: Gastropoda:
fossil
Mollusca: Gastropoda:
Nudibranchiata:
Okadaia elegans
Mollusca: Gastropoda:
Cymatiidae: Argobuccinum argus
Mollusca: Gastropoda:
Muricidae: Urosalpinx
Type of
excavator
Type of
excavation
burrower
burrow
coral exoskeletons
borer
borehole
borer
borehole
bivalve and brachiopod shells
spirorbid and serpulid
calcareous tubes
borer
borehole
borer
borer
borer
Mechanism of
penetration
mechanical; some
chemical?
Purpose of
excavation
Authors (this
Symposium)
residence, other?
Soliman
nutrition?
Sohl
chemicalmechanical?
nutrition?
Young
bivalve shell and
echinoderm tests
chemicalmechanical?
Day
borehole
shells of bivalves
and barnacles
mainly chemical;
some mechanical
does not generally
bore; other
species may
nutrition
borehole
shells of bivalves
and barnacles
mainly chemical;
some mechanical
nutrition
shells of molluscs
chemicalmechanical?
inject narcotic
into prey?
cinerea
Mollusca: Gastropoda:
Muricidae: Purpura
lapillus
Mollusca: Cephalopoda:
Octopus vulgaris
Nature of
substratum
borehole
o
c
Carriker
Nylen, et al.
Smarsh, et al.
taU, etal.
>
JO
SO
Arnold, et al.
Wodiusky
Type of
excavator
Type of
excavation
Mechanism of
penetration
calcareous skeletons
and rock
shells of oysters
chemical
burrow
molluscan and barnacle
shells
calcareous substrata
chemicalmechanical?
chemical?
burrower
burrow
chalk
mechanical?
borer
borehole
?
burrower
burrow
shell of pectinid
bivalves
coral: calcareous
rock
Lichens
burrower
Plaiyhelminthes: Turbellaria: Pseudoslylochus
oslreophagns
Plioronida: Phoronis
borer
borehole
burrower
burrow
burrower
• burrow
ova Us
Brachiopoda: Terebratula,
pedicle rootlets
Crustacea: Isopoda:
Spliaeroma pentodon
Mollusca: Gastropoda:
Capulus danieli
Echinodermata: Echinoidea
Nature of
substratum
chemical?
mechanical?
Purpose of
excavation
73
z
TABLE 2. Classification of known major taxa of calcibiocaviles not treated in this Symposium.
Penetrant
JO
Authors
nutrition?
residence?
to obtain access
to prey
residence,
other?
anchorage
Degelius (1962)
residence,
other?
feed on pectinid
food strings
residence,
other?
Barrows (1919)
z
o
Woelke (1957)
X
Marcus (1949)
Lonoy (1954)
Rudwick (1965)
Orr (1962)
Otter (1932)
3
COMPARATIVE CALCIBIOCAVITOLOGY
posium are classified in Table 1, while
known major groups not represented in
the Symposium are summarized in Table
2. The tables emphasize the broad distribution of the penetrating habit throughout the major divisions of the lower plants
and invertebrates. It is interesting to note
that embryophytes and chordates are not
represented. Whether rootlets of higher
plants are able to penetrate hard calcareous substrata in the manner described
for the pedicle rootlets of some brachiopods (Rudwick, 1965) and the holdfast
rhizoids of Fucus (Barnes and Topinka,
this Symposium) is not known, and poses
an interesting problem for research. So far
as we can determine, there are no calcibiocavitic vertebrates. DiSalvo (this Symposium) reports the first evidence that bacteria
are important in the breakdown of coral
skeletons, and Young (this Symposium) is
the first to report boring snails of the
subclass Opisthobranchia. The origin of
calcibiocavitation in past geologic periods
is discussed by Cameron; Seilacher; Macarovici; and Sohl (this Symposium); the
trace fossils (burrows and boreholes) indicate that the calcibiocavitic mechanism
had a very early beginning, and appeared
in several different major groups of organisms. The broad temporal, spatial, and systematic distribution of calcibiocavites, the
capacity for dissolution of shell by many
invertebrates in noncalcibiocavitic activities (Crenshaw and Neff; this Symposium;
Robertson, 1965), and the prominence of
osteoclastic activity in the vertebrates
(Schenk, Spiro, and Wiener, 1967), suggest
that calcibiocavitation may be a latent
fundamental characteristic of all protoplasm which has expressed itself from time
to time without regard to systematic position. That the nature of the environment
may be a factor in the development of the
penetrating habit, is suggested by the fact
that the great majority of calcibiocavitic
species are marine (indeed, cariogenic micro-organisms in oral cavities of vertebrates
function in a "marine-like" environment.
A conspicuous single exception in the Metazoa reported in this Symposium is the case
1015
of the fresh-water polychaete, Caobangia,
which burrows into the spire of the shell of
a fresh-water snail (Jones, this Symposium).
Boring invertebrates are not limited to
the phylum Mollusca (Table 2). The
turbellarian
flatworm,
Psendostylochus
(Woelke, 1957), excavates a small hole in
the shell of the oyster which causes the
valves to gape and provides the worm access to the soft tissues (compare with the
octopus, Arnold and Arnold; Wodinsky;
this Symposium). It is highly probable
that additional boring species will be discovered in other major taxa.
Burrowing organisms are divisible into
species in which the entire body resides
within the burrow (burrowing barnacles
and bivalves), and those where only a part
of the body is within the substratum (endolithic algae and clionid sponges, during
a phase of their life cycles).
SURVIVAL VALUE
From the standpoint of protection from
predators and extremes of natural physical
and chemical factors, residence in burrows
undoubtedly has survival value, while the
capacity to bore shell confers the advantage of entry into prey not otherwise generally accessible to predators. Cavitation of
biogenic calcareous substrata may provide
bacteria, fungi, and algae with nutrients
from the organic matrix which are not
otherwise available. The benefits, other
than protection, to endolithic algae burrowing in limestone have yet to be demonstrated. The reason for burrowing of clionid sponges in shell is likewise puzzling
since the life cycle can apparently be completed equally well in limestone. Possibly
occasional generations require trace substances present principally in the shell.
An extreme case of dependence on the
burrow for protection and support is that
of the burrowing barnacles whose valves
are replaced by the burrow walls (Tomlinson, this Symposium). The practice of adherence to the substratum by means of
holdfasts is probably an advantage in
1016
MELBOURNE R. CARRIKER AND EDMUND H. SMITH
maintaining position, but it is not known
why such species as Fucus (Barnes and
Topinka, this Symposium) and Terebratulina (Rudwick, 1965) send extensions into
the calcareous substratum when anchoring to it. This may be explained by the
fact that development of thalli and primary
rhizoids is enhanced on shell.
SUBSTRATA
The variety of substrata which may be
attacked by burrowers is very wide, and
encompasses every known type of calcareous plant and animal skeleton, the
organic matrix of these mineralized tissues,
and the three crystalline forms of CaCO:!
(calcite, aragonite, and vaterite), as well
as many kinds of naturally occurring calcareous rocks (ranging from soft chalk
to hard limestone) and the fine-grained
sedimentary rocks cemented by CaCO3
(Warme and Marshall; Craig, Dobkin,
Grimm, and Davidson; this Symposium).
Borers likewise exhibit a marked degree of
nonspecificity to the type of structural organization and mineralogy of the shell of
prey, the specificity, when present, being
directed instead to the external metabolites of the living prey (Wood, 1968).
This general lack of specificity among calcibiocavites to substrata is explained by the
fact that penetrative mechanisms attack
CaCO3, the common ingredient in nonbiogenic substrata, and, in addition, the periostracum and conchiolin common to shell.
The fine structure of biogenically formed,
calcareous substrata is described by Travis
and Gonsalves and by Kobayashi (this
Symposium). This information provides a
significant basis for interpretation of the
pathways of dissolution of shell by the
secretions of the penetrants (Travis and
Gonsalves; Cobb; Carriker; Smith; this
Symposium). The solubilizing effects of sea
water and of organic substances on some
of these substrata have been analyzed by
Pytkowicz, and by Kitano, Kanamori, and
Tokuyama (this Symposium), and likewise
should shed some light on the chemical
processes of excavation.
BEHAVIOR
Very little is known about the behavior
of most calcibiocavites during penetration.
It varies, almost as widely as there are
species of penetrants (Cobb; Rice; Haigler; Smith; Young; Carriker; Arnold
and Arnold; Wodinsky; this Symposium).
To date, the excavating behavior of Urosalpinx (Carriker), Penitella (Smith), and
Octopus (Arnold and Arnold; Wodinsky)
has received the most attention. It is suggested in the literature that some calcizoocavities (the isopod, Sphaeroma, Barrows, 1919; some echinoids, Otter, 1932)
excavate entirely by mechanical means in
soft substrata. Penetration by most invertebrates, however, involves a combination of
chemical and mechanical activity. The significance of each of these two processes is
being clarified by research on such genera
as Cliona, Polydora, Urosalpinx, and Penitella. In the mechanical aspects of excavation, penetrants employ a variety of hard
biogenic structures such as bristles, hooks,
spines, papillae, shields, teeth, valvular
edges and surfaces, and radular cusps.
These abrade the surface of the substratum
in varying degrees after it is weakened by
secretions released by the organisms. The
extent to which these structures are necessary in the excavating process by most species is unknown. In Urosalpinx (Carriker,
this Symposium) and in Penitella (Smith,
this Symposium), for example, penetration
is achieved primarily by chemical dissolution of the shell, and radulae and valves,
respectively, play a very minor role in excavation. In such organisms as bacteria,
algae, fungi, lichens, Psendostylochus, and
Terebratulina, where no hard parts appear
to play a part, the process seems to be
entirely chemical.
ISOLATION OF THE PENETRATION
In both the burrowing and boring species examined to date, the penetrant isolates the site of excavation from environmental water during the chemical phase of
penetration using a part of its body, a
secreted mucous envelope, a capsule, or
COMPARATIVE CALCIBIOCAVITOLOCY
some other covering, thereby eliminating
or reducing dilution of its secretion. As the
excavation is deepened, isolation is further enhanced. Endolithic algae, for example, completely fill burrows with their filaments; penetrating cells of Cliona press
closely against the substratum; the mantle
of Penitella is in contact with the substratum; and the accessory boring organ of
Urosalpinx closely fills the borehole. In
these organisms, which may be representative of most chemical penetrants in this
regard, the relatively undiluted secreted
solvent probably acts directly on the substrate, radically altering the microenvironment at the interface of secretory
cells and calcareous substratum. Kitano,
Kanamori, and Tokuyama (this Symposium) showed the extent to which organic
substances may affect the solubility of crystalline carbonate. The degree to which isolation is critical in the effective functioning of the dissolvent mechanism in all penetrants is unknown, but it is certain that
the reactants must be kept at a reasonably
high concentration for solubilization to
proceed at an efficient rate, and in this
sense exclusion of sea water should assist.
Pytkowicz (this Symposium) stresses that
sea water must be undersaturated with
calcium for solution of CaCO 3 to occur. In
general, ocean waters are supersaturated
in the upper layers and undersaturated at
depth, although the degree of saturation of
these waters may not be representative of
conditions immediately adjacent to organisms where release of CO;, and other catabolic products may alter the pH. As pointed out by Crenshaw (personal communication), sea-water models pertaining to
CaCO. r equilibrium are constructed on the
basis that the quantity of the solid phase
is infinitely small with respect to the
solvent; the reverse is closer to conditions
in penetrating systems, and sea-water models are consequently inapplicable. In any
case, the degree of saturation of sea water
in the environment is probably not a major factor in penetration, as at least at the
time of chemical activity the penetrant dis-
1017
places sea water in the site of penetration
with a part of its body.
CHEM ICAL MECHANISMS
Although it has been demonstrated experimentally that chemical dissolution is
carried out by some penetrants (bacteria,
DiSalvo; Cliona, Cobb; Polydora, Haigler;
Penilella, Smith; Argobuccinum, Day; and
Urosalpinx, Carriker; this Symposium),
little is known about the physiology of
substrate-dissolution.
Acids
(Carriker,
Charlton, Van Zandt, 1967), chelating
agents (Jenkins and Dawes, 1963), and,
most recently, specific enzymes (carbonic
anhydrase: Smarsh, Chauncey, Carriker,
and Person; Chetail and Fourni^; this
Symposium), as well as nonspecific esterases, acid phosphatase, alkaline phosphatase, decarboxylases, and transaminases
(Chauncey, Smarsh, Carriker, and Person,
pers. comm.) have been indicated as possible dissolvent mechanisms.
Conjectures on the dissolution of CaCCv
substrates by secretion of carbonic acid
are frequent in the calcibiocavitological literature. Crenshaw (pers. comm.), after noting that Kitano showed that
CaCO-i-solubility is increased less than
20-fold by increasing the CO2-tension 1
atm, pointed out that coccoliths can be
dissolved in sea water with CO2 only when
the CO2-tension approaches 1 atm. He
noted further that the only reported measurements of pH at the site of chemical
penetration gave values in the range of 3.8
to 4.1 {Urosalpinx: Carriker, Charlton,
and Van Zandt, 1967), and that these pH
values cannot be reached by the secretion
of CO2, for when sea water is titrated with
COo the pH asymptotically approaches a
value of 6 up to 1 atm of CO2 (Beyers,
Larimer, Odum, Parker, and Armstrong,
1963). Crenshaw believes, therefore, that
dissolution of shell by carbonic acid is not
possible. However, as has been suggested,
calcibiocavitic organisms more or less effectively exclude sea water from the site of
penetration, and the buffering action of
sea water would consequently be minimal.
1018
MELBOURNE R. CARRIKER AND EDMUND H. SMITH
Furthermore, measurements of pH are
seriously altered in viscous media as a result of the so-called "suspension effect"
(Bates, 1964), and this raises the question
as to the applicability of pH values in
homogeneous aqueous systems to the viscous heterogeneous suspensions that characterize penetrating secretions of such calcizoocavites as Urosalpinx.
Information from different investigators
suggests some variation in the chemical
mechanisms in different species of penetrants, but the results are too preliminary
to permit erection of a hypothesis on either
a common mechanism fundamental to all
penetrants, or a variety of chemical
mechanisms for the different taxa. Crenshaw and Neff (this Symposium) demonstrated that succinic acid is produced
anaerobically at the mantle-shell interface
of the bivalve, Mercenaria, when the animal is closed, and that this acid is neutralized by dissolution of previously deposited
shell at this interface. Silen (1947; Soule
and Soule, this Symposium) concluded
that phosphoric acid is used in penetration
by burrowing bryozoans, because he
found more phosphate ions in invaded
shells than in normal ones. Day (this Symposium) in a study of the shell-dissolving
secretion of the snail, Argobuccinum,
found that no enzymes are involved in the
dissolution, but that H2SO4 is present
and accounts for 67% of the CaCO3-dissolving activity of the secretion; the remaining
solubilization of the shell is achieved by
some other unidentified component which
may be a chelating agent. The secretion
also contains a narcotic which relaxes
prey, and is suggestive of the substance
injected into prey by Octopus, and possibly
by Pseudostylochus. Chetail and Fournie
(this Symposium) postulate involvement
of carbonic anhydrase in shell-penetration
by the snail, Purpura, because of inactivation of boring activity by Diamox and acceleration of boring by CO2. They suggest
further that H+ ions released by the active
boring organ may be exchanged for Ca+ +
ions, and that in addition Na+ and K+
ions may also be involved in exchange.
Smarsh, Chauncey, Carriker, and Person
(this Symposium) have confirmed the reliability of specific histochemical procedures
for the localization of carbonic anhydrase
and have shown that this enzyme is
present in the accessory boring organ of
Urosalpinx. In addition, they have indicated that there is present a water-soluble,
acetone-precipitable chelator in the microvillar area of the accessory boring organ.
Other data from these investigators (pers.
comm.) indicate that chemical action on
the CaCO3-substrate is a multiphasic, enzyme-dependent process which initially involves the dissolution of the CaCO3 by a
mineral acid and subsequent chelation of
the released calcium ions.
Although nothing has yet been reported
on the chemical method of solubilization
of the organic matrix of shell by calcibiocavites, a clue may be had from the observations of Travis and Gonsalves (this Symposium). They found in thin sections that
considerable amounts of the organic
prismatic sheaths solubilize with prolonged
treatment in dilute concentrations of
EDTA, and that the intraprismatic matrices are not only extremely soluble in
these concentrations of EDTA but also dissolve in water over a period of 1-2 hr. In
addition to their suggestion that conchiolinase-like enzymes, not yet identified in the
accessory boring organ or its secretion, may
be a significant link in the chemical
mechanism of penetration, it is possible a
chelating agent is also part of the mechanism.
The manner of removal of Ca++ and
CO3=ions and the dissolved products of
the organic matrix of biogenic substrata
from the penetration may be solved in different ways by different species. In burrowing organisms like the endolithic algae,
it is likely that transport of ions out of the
burrow may occur across the plasma
membrane and through the organism to
the exterior, as there are no other obvious
outlets. In the case of clionid sponges
which remove large quantities of substratum relative to the volume of the burrowing sponge, only a small amount of the
COMPARATIVE CALCIBIOCAVITOLOCY
substratum is dissolved and the remainder
is ejected as solid fragments (chips) by
way of the excurrent water canals; overall,
this type of excavation may be more
economical and require less energy than
would that by solubilization alone. In
higher invertebrate penetrants like Polydora, Penitella, and Urosalpinx, dissolved products may be flushed out of the
penetration with sea water by movements
of the body or of the boring organs between periods of chemical activity, as well
as transported across plasma membranes
into the organism in exchange for other
ions. Further research will undoubtedly
disclose additional possibilities for discharge of these products in other species.
In the deep sea, solution of CaCO3 occurs more readily than at sea level because
of low temperatures, high pressures, and
undersaturation of calcium (Pytkowicz,
this Symposium). If these factors favor
penetration, calcizoocavites in the deep sea
(Carriker, 1961) should function more
efficiently than those in surface waters. It is
an attractive research problem which has
not yet been undertaken. On the other
hand, solubility of CaCO3 increases with
decreasing salinities, and so one would expect that calcibiocavitism would increase
in frequency up estuaries into fresh water.
Surprisingly, if available information is
representative, quite the converse is true,
and calcibiocavites are extremely uncommon in the fresh-water environment. This
apparent paradox presents another fascinating problem for research.
PATHWAYS OF CHEMICAL PENETRATION
Recent research suggests some of the pathways of solvents in the chemical penetration of substrates by organisms. Chemical
dissolution of the relatively hard shell of
some bivalve molluscs, for example, seems
to take place initially through the framework of the non-mineralized organic matrix (Travis and Gonsalves; Carriker; this
Symposium), the thick, organic, prismsheaths providing structural pathways for
the passage of the solvents. As the sheaths
1019
are dissolved, the solvent passes through
the intraprismatic matrix which surrounds
individual inorganic crystals and solubilization advances to include the mineral
phase. Dissolution of relatively soft molluscan shell presents a different picture (Carriker, this Symposium), and the pathways
are not yet evident. The microcanals described by Kobayashi (this Symposium) in
the valves of some bivalve molluscs should
provide excellent avenues for the penetration of the solubilizing secretion, and no
doubt they may, but valves which lack
them are also penetrated readily, although
the rate of penetration in the two types of
shell is not known. DiSalvo (this Symposium) has demonstrated that bacteria break
down coral by attacking the organic matrix
rather than the CaCCycrystals; it is probable fungi proceed in the same manner,
but this remains to be investigated. In burrowing Iceland spar, which lacks the organic matrix, the terminal cells of endolithic
filaments of some algae (Golubic, this
Symposium) follow the lines of crystal
twinning so that the walls of the burrows
are coincident with the main cleavage
planes of the calcite crystals.
These several observations point out
that periostracum, conchiolin, and biogenic and nonbiogenic crystalline CaCO3 are
all penetrated by calcibiocavites, indiscriminately by burrowers, and in borers limited
to shell of prey. In the case of shell, solubilization involves both crystalline CaCO3
and organic materials, and consequently
the frequently used terms, "decalcification" and "demineralization", are inappropriate as they apply only to destruction of
the mineral fractions; the term "shelldissolution" more suitably describes the
total process.
PROTECTION OF PENETRATING TISSUES
How the living tissues of calcibiocavites
are protected from the secretions utilized
in dissolution of the substrates is unknown. It has already been pointed out
that many penetrants employ hard parts
for mechanical attrition of the substratum,
1020
MELBOURNE R. CARRIKF.R AND EDMUND H. SMITH
and that these structures become abraded
with use, but it is unclear whether these
structures are shielded from solubilization
by the penetrating secretion.
THE FUTURE
When substantially completed in the far
future, the body of knowledge in calcibiocavitology will include the discovery of
many more species of penetrating organisms; the comprehensive treatment of the
systematics, biogeography, ecology, behavior, paleontology, and evolution of known
taxa; the structure, physiology, and development of structures used in penetration; the physical and biochemical
mechanisms of penetration; and the structure of the substrata and the effect of the
penetrating organs and their secretions on
these. Unquestionably, the diversity of
morphological and behavioral mechanisms
will be shown to be considerably broader
than already disclosed; however, it is likely
that chemical mechanisms will be less
varied, principally because the major components of substrata are CaCO3 and an
organic matrix. The degree of diversification of chemical mechanisms will probably
in large part reflect chemical variation of
the organic framework of shell, and something of the range of this has been under
investigation recently (Ghiselin, Degens,
Spencer, and Parker, 1967).
We hope that this Symposium will serve
as a stimulus for much more research on
all phases of comparative calcibiocavitology, particularly at behavioral, ultrastructural, physiological, and biochemical levels.
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