ACTA UNIVERSITATIS UPSALIENSIS Abstracts of Uppsala Dissertations from the Faculty of Science

680

ASPECTS OF THE FUNCTIONAL MORPHOLOGY

OF FOSSIL AND LIVING INVERTEBRATES

(BIV ALVES AND DECAPODS)

by

ENRICO SA V AZZI

UPPSALA 1983

2 Enrico Savazzi

INTROD UCTION

This publication summarizes the papers in functional morphology

previously published by the author (see below), and provides an

overview of the general themes and research guidelines followed.

Unpublished data relevant to the discussion and further research

possibilities connected with the subject are briefly covered. The

present paper has been produced in fulfillment of the requirements for

doctoral dissertations at Uppsala University, Sweden.

The studies presented here deal with two distinct basic themes in

functiona 1 JIDrpho logy. The first of these concerns burrowing

sculptures; i. e., external sculptural patterns that aid hard-shelled

invertebrates in burrowing through soft substrates, and which are

compared among different taxonomic groups. The phylogenetic,

developmental and constructional constraints of each group impose

different limitations to the optimization of burrowing sculptures

(Savazzi 198lb, 1982a, 1982b, Savazzi, Jefferies & Signor 1 982).

The second theme deals with the adaptive strategies of bivalves,

originally adapted to life on or within solid substrates, and which

evolved secondarily into soft-bottom dwellers (Savazzi 198la, 1982c,

1982d and unpublished manuscript; Chinzei, Savazzi & Seilacher 1982).

These papers show also that only a limited number of conceptual tools

is available for the study of functional morphology in macro­

invertebrates.

HETHODS IN F UNCTIONAL MORPHOLOGY

When studying the relationships between morphological characters of an

organism and its immediately surrounding ecosystem, a working

hypothesis is usually formulated about the adaptive value of an

observed morphology. The functional hypothesis can subsequently be

tested in a variety of ways (see below). A less immediate but equally

valid approach (C. R. C. Paul (Liverpool), verbal communication 1980)

Aspects of functional morphology 3

is to individuate first one or more functions required by the organism,

and subsequently look for the corresponding morphological adaptations.

In this context, a character is defined as functional if it can be

shown to increase the adaptiveness of the organism as a whole. Since

an absolute statement of non-functionality of a morphological character

is not falsifiable (it cannot be excluded that a function will

eventually be found; Reif 1975, 1982), the definition of functionality

is often restricted to characters bearing a direct relationship with

the 1 i fe habits and eco 1 ogi ea 1 niche of the organism. Thus, the

colour pattern of some burrowing bivalves has been defined as non­

functional (Seilacher 1972), since it has no conceivable effect in

enhancing the fitness of the organism to the infaunal life habit.

In this restricted sense, a statement of non-functionality does not

imply any connotation of neutralist evolution (see dicussion in Reif

1982). Contrary to the opinion of Gould & Lewontin (1979), I do not

accept the idea that the formulation and testing of functional

hypotheses presupposes the a priori assumption of adaptiveness of the

organism. Rather, adaptiveness itself is testable as part of the

working hypothesis (Reif 1932, and below). However, the indirect

inference of function from morphology in fossils does presuppose the

acceptance of a selectionist point of view, and is not compatible with

strongly neutralist theories (Lewontin 1978, Reif 1982).

In living organisms, a functional hypothesis may often be directly

testable by observing the result of experimental modifications of

selected morphological characters and/or environmental conditions.

When modification of the experimental conditions is not feasible

(typically, when conditions cannot be altered singly), indirect

informations can still be collected by monitoring the organism's

activity by unobtrusive techniques. The typical case is repr·esented by

complex behavioural changes induced by experimental �Iterations of

JIDrphological characters. For examples of these two methods, see

Savazzi 1982a and 1982b, respectively).

The methods of functional analysis in fossils must obviously be less

direct, but the same basic principles can be used. In fact, the

indirect methods developed by palaeobiologists can often be profitably

applied to living organisms as well. These methods can be summarized

as follows (a somewhat different scheme was proposed by Reif 1982).

4 Enriao Savazzi

a) Comparison of fossil organisms with Recent counterparts possessing

assumedly analogous or homologous characters that are susceptible to

direct testing of functional hypotheses.

b) Comparison of morphological characters with one or more

alternative mechanical analogues (paradigms) designed to provide the

hypothesized function with maximum efficiency (Rudwick 1964) .

c) Experiments with actual fossil specimens or physical models to

test the properties of morphological characters.

d) Informations on the life habits, ontogeny and ecological

relationships derived from the occurrence and preservation of fossil

organisms, traces of predation and parasitism, composition of the

thanatocoenosis and sedimentological evidence inferred from the

enclosing rock.

While these methods may be applied to single characters, the

conclusions should take into account the organism as a whole (cf.

Savazzi l982a) . The comparison of fossil organisms with Recent

counterparts can only be as good as the extent of our knowledge of the

degree of similarity and the understanding of organs and soft parts

normally not preserved in fossils. The validity of the actualistic or

uniformitarian principle has to be assumed. Obviously, the method is

least useful with organisms lacking taxonomically related Recent

representatives. The paradigm method (b) , as presented by Carter

(1967) consists of four distinct steps (see also Paul 1975) :

1) A functional hypothesis is made, 2) a theoretical model (paradigm)

is designed to provide the hypothesized function with maximum

efficiency (constraints due to the materials available are allowed for

at this stage) , 3) the actual organism is compared with the paradigm,

4) the functional hypothesis is accepted or rejected according to the

goodness of fit of the actual morphology to the paradigm. Alternative

paradigms based on different mechanical principles to provide the same

function can be tested.

While a good fit between the paradigm and the real organism is a

strong suggestion in favour of the functional hypothesis, a bad fit is

not necessarily an indication of non-functionality. A particular

morphology need not necessarily be optimized at an engineering scale in

order to provide the function at the level required by the organism.

r�oreover, trade-offs between different or contrasting functional needs

Aspects of functionaZ morphoZogy 5

may prevent the evolution of the optimal morphology. Trade-offs may

occur also in favour of non-morphological characters (e. g., fertility,

growth rate) which may be difficult or impossible to assess in fossils.

It has been suggested that constraints may be taken into account

when selecting the paradigm (Cowen 1979). However, phylogenetic and

constructional constraints are often inferred from the general lack of

certain features in a taxonomic group (cf. Signor 1982a). Therefore,

allowing for these constraints while selecting the paradigm may lead

to a circular reasoning (circuZue vitiosus). Signor (1982a) rejects

the paradigm method for this reason, and because a negative outcome of

the comparison of the organism with the paradigm does not necessarily

falsify a general hypothesis of functionality. He further proposes to

adopt constructional morphology (see following section) in place of

the paradigm method. I do not agree with Signor that constructional

morphology can be regarded as a substitute to the paradigm method

(or to any of the other methods here discussed). Furthermore,

falsification of the functional hypothesis is not the necessary

outcome of a negative result in any of the approaches listed above, so

that there appears to be no flawless substitute for the paradigm

method. Therefore, I prefer to retain it, allowing only for constraints

dictated by concurrent functions and coadaptive characters, which can

be incorporated in the functional hypothesis. In this way, a lack of

compliance with the paradigm, while not excluding a general hypothesis

of fu�ctionality, does, indeed, exclude that the hypothesized function

is carried out in the way envisioned by the paradigm. Constructional

and phylogenetic constraints can be considered later on, to explain

why the actual morphology does not comply with the paradigm.

While the choice of the appropriate paradigm presupposes a fairly

good understanding of the laws or principles involved, the use of

fossil specimens or physical models in actual experiments (method c)

is suitable when the engineering prohlem of designing a paradigm is

too complex, or the principles involved are little understood. Since

the inferential process is e;sentially the opposite to that of the

paradigm method, I prefer to regard these two approaches as separate.

Weak points of this latter approach are that it can be applied with

confidence only to skeletal parts, and that only passive properties

are accurately simulated. Ideal fields for the application of this

6 Enrico Savazzi

method are problems in fluidodynamics, such as the effect of shell

sculpture on erosional scour around the exposed shell regions (Stanley

1977, 1981, Bottjer & Carter 1980) or passive re-orientation of

organisms (Fisher 1977, Savazzi l982c) . This method can be also

successfully used to study active properties of morphological traits,

such as the effect of shell sculpture on the burrowing process in

bivalves (Stanley 1975, 1977) . In this case, the resulting

oversimplification in reconstructing and simulating the behaviour of

the organism may cause the results to be not directly comparable with

biological data.

Evidence derived from.traces of predation, parasitism or association

with other organisms and from taphonomical (Efremov 1940) aspects

(method d) can be usefully compared with data from Recent organisms.

This method is most useful for assessing the life habits of fossils in

relation to the immediately surrounding habitat. For instance,

information on the burrowing depth and shell orientation of infaunal

bivalves can be obtained from the presence of sessile epibionts on the

exposed shell regions and from the pattern of repaired damage to the

shell margins (Savazzi l98la, 1982b, l982c, and manuscript) . Care

must be taken to identify all post-mortem and preservational

alterations.

It is evident from the above discussion that the different approaches

to functional morphology are not mutually exclusive, and that they

should rather be used in conjunction with each other. The reasoning

involved is not circular, since new data are collected along the way

by testing and refining the functional hypothesis.

CONSTRUCTIONAL t-10RPHOLOGY

As defined by Seilacher (1970), constructional morphology is an attempt

to explain the morphology of an organism as the interaction of three

factors ("aspects") : the phylogenetic heritage of the organism, its

constructional and developmental mechanisms (including the morphogenetic

programmes, the properties of the materials involved and ecophenotypic

characters) , and its functional morphology in relation to the life

Aspects of functionaL TN)rphotogy 7

habits and ecosystem. As examples of this method, see Savazzi (1981a,

1981b, 1982c, 1982d, and manuscript). Raup (1971) proposed to add

chance (in a neutralist sense) and ecophenotypic factors as separate

aspects. The inherent difficulty of including random-walk evolution

or other neutralist concepts is that their existence cannot be directly

derived from the observed morphology (except perhaps through

statistical treatment of large data sets). Most of the further aspects

proposed by Hickman (1980) can be grouped under the general heading of

constructional and developmental mechanisms. In the present and

associated papers, the original definition of constructional morphology

is adhered to.

I do not agree with Signor (1982a) in regarding constructional

morphology as an alternative to other methods in functional morphology.

Given its original definition, constructional morphology is rather a

broader attempt to explain morphology, employing functional morphology

as one of its basic tools.

BURROWING SCULPTURES

Organisms with mineralized skeletal parts, possessing a high

fossilization potential, are favourite subjects for studies in

functional morphology. In particular, the exoskeleton of invertebrates,

being in direct contact or close proximity with the environment, is

likely to possess morphological characters functionally related with

the life habits of the organism. This is especially true of burrowing

or boring organisms, since the forces necessary to penetrate the medium

are high enough to require special adaptations. In the present context,

the term burrowing is used restrictively to indicate movement through

loose sediments of variable grain-size and cohesiveness, but in which

the sediment particles are never cemented to each other. The term

boring is reserved for locomotion through a solid substrate, whose

shear force may easily approach the mechanical strength of the boring

parts. Actually, in most cases, the boring activity simply provides a

place for the growth of the organism. Although the distinction between

burrowing and boring is to a certain extent artificial, it complies

8 En:rico Savazzi

well with the observed variety of locomotory patterns involved.

The types of bUrrowing processes were summarized by Seilacher (l982a),

mostly according to the nature of the appendages involved. These

processes can be divided into two basic types: eontinuous, in which the

·organism proceeds through the substrate at a steady rate (e. g.,

burrowing echinoids; see Ghiold 1 979, 1982, and Ghiold & Seilacher

1 982), and intermittent, in which one part of the body acts as an

anchor against backslippage, while the actively burrowing part probes

forward through the sediment. The role of the two parts is

subsequently exchanged in the next phase of the burrowing process.

Together with other auxiliary movements, the two complementary phases

constitute a burrowing sequence (Trueman & Ansell lg69; cf. also

Savazzi 1 982a). The anterior and posterior parts of the organism

active in the burrowing process were originally called retraction and

penetration anchor, respectively (Trueman & Ansell ' 1 969). Occasionally,

these two parts are located side by side (e. g., the dorsal and ventral

surfaces of the Recent reptile OphisaUI'US; Frey 1982).

All the organisms considered in the present connection employ (or

are supposed to) an intermittent burrowing process. The two burrowing

anchors can be either soft (foot of bivalves, whole body of polychaetes)

or rigid (mollusc shell, crustacean cuticle). Basically, progression

through the substrate is achieved by alternately shifting the maximum

friction against the substrate between the two anchors. While a soft

organ can be alternately inflated and contracted (e. g., the bivalve

foot), rigid parts may have a fixed volume (the valves of the bivalve

shell can be adducted together.to reduce the cross-sectional area, but

in gastropods, the shell is a single unit). Passive morphological

features may aid in burrowing, provided that they exert a consistently

different friction in opposite directions. Based on these requirements,

a paradigm for burrowing sculptures can be designed. Stanley (1969)

observed that several Recent bivalve species possess growth-unconformable

ridges (i. e., neither commarginal (="concentric") nor radial), which

are oriented perpendicularly to the burrowing direction and are

terrace- or sawtooth-shaped in cross-section. Since the steeper side

of these ridges faces away from the burrowing direction, he suggested

that these ridges also possess a lower grade of friction when moved in

the burrowing direction (thus not hindering forward movement) than in

Aspeets of funetional morphology 9

the opposite direction. The higher friction in the opposite direction

would be functional in bracing the shell against the substrate while

the foot probes forward. The hypothesis was further supported by

observations on living bivalves showing that the orientation of the

terrace-lines was in agreement with the burrowing direction. In

defining the paradigm for burrowing sculptures, Seilacher (1973) used

observations on a wide range of burrowing invertebrates. The

requirements of this paradigm were summarized by Savazzi (1981b, 1982a,

1982b) and Savazzi, Jefferies and Signor (1982). The compliance of

the actual organisms with the paradigm was so good, that "burrowing

sculptures" came to be regarded almost as a synonym of "terrace

sculptures" (evidence for this statement can be found in Seilacher

1972, 1973, 1976, Schmalfuss 1976b, 1978a). Terrace patterns with

different functions have been described (Schmalfuss 1978a), and a

variety of functions have been hypothesized for other types of

sculptures (e. g., Schma lfuss 1975, 1977, 1978b), but evidence fot·

burrowing sculptures totally different from terraces came only recently

(Stanley 1981, Savazzi 1982a). Reasons for this bias may be found in

the fact that comparisons with a range of actual organisms was used

in the early phase of choosing the characters of the paradigm (which

should rather be derived from theoretical principles). A tendency to

treat burrowing sculptures independently of the context of the whole

organism may also be responsible.

In decapod crustaceans, sculptural features interpreted as burrowing

sculptures range from asymmetrical tubercles (Savazzi 1982b) to fully

formed terrace lines (Seilacher 1961, 1973, 1976, Schmalfuss 1978a,

Savazzi 1981b, 1982b, Savazzi, Jefferies & Signor 1982; see Schmalfuss

1975, 1981 on other crustaceans). For the reasons expressed above,

sculptural patterns differing from terraces have only recently received

attention. Future research may show that they occm· far more

frequently than well-developed terraces (Savazzi, unpublished data).

It is easy to imagine an evolutionary process leading from isolated

asymmetrical tubercles to terrace-shaped ridges formed by the fusion

of transversely aligned tubercles (Savazzi 198lb, 1982b). In most

cases, this is further suggested by the facts that the edge of the

terraces is crenulated (Savazzi l98lb: Fig. 2; 1982b: Figs. 4, 8, 11),

and that the terraces in the anomuran Emerita increase ontogenetically

10 Enrico Savazzi

in length by the addition of new crenulations at the sides (Seilacher

1973, 1976). The terraces of the brachyuran Ranina (Lophoranina) are

identical, in cross-section and general appear·ance, to the randomly

scattered isolated tubercles of Ranina (s. s.) , from which they likely

evolved (Savazzi 198lb and unpublished). Also, in the brachyuran

Corystes the well-formed terraces in the posterior region of the

carapace (where they are most needed for burrowing) grade into shorter

terraces and isolated tubercles in the anterior region (Savazzi 1982b).

The smoothly edged terraces present in part of the grapsid crabs may

have evolved through a different evolutionary pathway (Savazzi,

unpublished). These terraces are not burrowing sculptures, but are

functional in increasing friction against the substrate when the crabs

wedge themselves in rock crevices. The increased friction prevents them

from being extracted by predators (Schmalfuss 1978a).

Since the physical size of the burrowing sculptures is related to the

grain-size of the surrounding sediment, the physical size of the

burrowing ribs (in particular, their relief and spacing) should remain

constant during growth ("allometric densing" of Seilacher 1973). This

requires an allometric growth process. Failure to comply with this

aspect of the paradigm in the brachyuran Ranina (Lophoranina) may

indicate the existence of constructional or phylogenetic constraints

(Savazzi 198lb, 1982b). Experiments with artificial models of terrace

patterns (Savazzi 198lb) show that, although apparently lacking the

capability of introducing new terraces among preexisting ones during

growth, Lophoranina nonetheless underwent ontogenetic adjustments to

partially maintain the efficiency of the burrowing sculptures. The

randomly distributed tubercles in Ranina (s. s. ) , unlike the

asymmetrical tubercles in other crabs (cf. Savazzi l982b), are

approximately five times longer (in the burrowing direction) than wide.

Placing these tubercles side by side to form terraces running from one

side of the carapace to the other, as seen in Lophoranina (including

juveniles) would leave no space for further introduction of sculptural

elements in the way observed in Emerita (Seilacher 1973) and Corystes

(Savazzi 1982b) (Savazzi, unpublished).

Many burrowing bivalves show a variety of sculptural traits that do

not comply with the paradigm for burrowing sculptures. Other functions

of bivalve sculptures are well documented (mechanical strengthening:

Aspects of functiona� morpho�ogy 11

Kauffman 1969; retardation of scour around the exposed or shallowly

buried posterior shell margins: Stanley 1977, 1981, Bottjer & Carter

1980; camouflage and preventing or favouring the attachment of epibionts

to exposed shell regions: Stanley 1970, Bottjer & Carter 1980;

deterring predators: Carter 1967; facilitating the respiratory activity

by increasing the length of the commissure or by sustaining induced

flow: Stanley 1970, Paul 1975), but experiments with living bivalves

(Stanley 1981, Savazzi 1982) show that also sculptures not optimally

designed as burrowing ribs can indeed be functional in burrowing.

The reason why sculptural traits that are extremely coarse (with

respect to the grain-size of the sediment) and lacking any visible

reason for exerting a different frictional force in opposite directions

should be more efficient than a smooth surface (as shown by the actual

experiments) lies in other coadaptive characters of the burrowing

process. The hydraulic pumping action that complements the mechanical

rocking of the shell during the burrowing process (see Stanley 1975,

1977, Savazzi 1982a) periodically changes the physical properties of

the surrounding sediment. Therefore, the mechanical asymmetry of the

sculpture is substituted by a temporary asymmetry in the properties of

Lhe sediment, which change in different moments of the burrowing

sequence. Burrowing sculptures have also been described in gastropods

(Signor 1980, l982b), trilobites (Schmalfuss 1981; see Miller 1975 for

a totally different interpretation) and calcichordates (Savazzi,

Jeffet·ies & Signor 1982). Terrace patterns in obolid inarticulate

brachiopods appear to satisfy all the requirements of the paradigm

for burrowing sculptures (Seilacher 1973). However, the steep faces

of the terraces are directed away from the peduncule, suggesting that

they burrowed with the distal commissure posteriormost. Actually,

their closest Recent counterparts, the Lingulidae, are known to burrow

in the opposite direction (Thayer & Steele-Petrovic 1975j. This may

suggest either a totally different burrowing mechanism for the Obolidae,

or a function of the terraces other than burrow·i ng.

According to the interpretation offered by Schmalfuss (1981), the

terraces on the ventral side of trilobites are used to prevent sediment

particles from sliding in the cavity excavated by the appendages under

the body to allow filter feeding, and accordingly are directed outwards

along the entire perimeter of the ventral surface. Since these

12 Enrico Savazzi

terraces do not have to move in opposite directions with respect to

the sediment, as true burrowing sculptures do, their requirements

should be different. In fact, the ventral terraces in trilobites seem

to be consistently more projecting than the terraces on the dorsal

side (which are true burrowing sculptures facing the posterior

direction) . It is interesting to note that, in bivalves that burrow

with the commissure plane horizontal (e. g., Tellinidae) , the terraces

on the lowermost lying valve are actually less conspicuous than on the

dorsa 1 one, probably in order to compensate for the difference in 1 oad

exerted by the sediment (Seilacher 1972, 1973, Savazzi 198la) .

In the Recent crabs Gecarcinus and Ocypode, terraces occur on the

legs and, in Gecar>cinus, along the sides of the carapace. Both these

genera excavate burrows in subaerial environments. The terraces in

Gecarcinus were said by Schmalfuss (1978a) to be functional in

preventing sediment being carried out of the burrow from slipping

between the first leg and the terraced ventro-lateral region of the

carapace. Observations on both genera in their natural environment in

Bermuda and on live specimens in the laboratory (Savazzi, unpublished)

show that the sediment being carried out from the burrow is kept

pressed between the first pair of legs and the mouthparts, and is

never in contact with the terraced regions. It was possible to show

that the terraces in these crabs become functional in wedging the

organism against the wall of the burrow when threatened by a predator

or an intruder. The wedging behaviour in adult Ocypode is usually

abandoned in favour of running or fighting, and the terraces are

accordingly degenerated with respect to juveniles of the same species

(in particular, they tend to loose the asymmetrical edge and to become

rounded in cross-section) . Further studies may show other differences

from true burrowing sculptures. It is interesting to note that in

Gecai'cinus the terraces in a restricted area of the pteri gas tomi a·l

region are secondarily modified into a stridulatory apparatus (Klaassen

1973) . Terrace patterns in other groups (e. g. , eurypterids) still

await detailed investigation.

SECONDARY SOFT-BOTTOM BIVALVES

Aspects of functional morphology 13

Bivalves are believed to have originally evolved from rostroconch

ancestors. Since the Palaeozoic, a variety of forms have become

secondarily adapted to life on, or within, solid substrates (Stanley

1968, 1972, Pojeta & Palmer 1976) . The hard bottoms offer the principal

advantages of being mechanically stable and of providing concealment

and mechanical protection against predators and natural agents (at

least in nestling and boring forms) . Better aereation may be of

relevance in certain environments. Most hard-bottom bivalves have

entirely lost their locomotory abilities, at least in the adults, and

are directly cemented or byssally attached to the substrate.

Mechanically and/or chemically boring forms have evolved in several

lineages (cf. Purchon 1954, 1955, Yonge 1955, Pojeta & Palmer 1976,

Roder 1977, Carter 1978, Kleemann 1980, Savazzi 1980, 1982c, 1982d,

1982e) . A number of other taxa have adapted as nestlers in empty

boreholes. Usually, the extent of the morphological changes resulting

from the adaptations to the hard bottoms prevented the return to a

free-burrowing or endobyssate habit comparable with that of their

soft-bottom ancestors. Therefore, the secondary return of these

organisms to the soft bottoms is particularly interesting, since it

can be expected that the different adaptive strategies would channel

evnl ut.ion into a variety of areas unexploi ted by primary soft-bottom

dwellers.

The soft-bottoms environments are mostly characterized by their

intrinsic instability as compared with solid substrates. A

soft-bottom dweller incapable of active movements should therefore

exploit one or more passive strategies in order to maintain or

re-establish a suitable life position (cf. Savazzi 1982c, Seilacher

1982a, Chinzei, Savazzi & Seilacher 1982) . These adaptive strategies

are summarized as follows:

1) attachment to solid objects (shells, wood, seaweeds) ;

2) building a structure so heavy or deeply anchored that it is

unlikely to be disturbed in the first instance;

3) adopting a morphology whose geometrical properties facilitate

the re-establishment of the life position by gravity and/or water

14 Enriao Savazzi

currents;

4) association with an actively moving organism which assures a life

position suitable for the host.

Solutions 1) and 4) are often accompanied by a reduction in adult size.

The first solution requires few morphological changes with respect to

the hard-bottom ancestors, and appears to have often been used as a

stepping evolutionary mechanism into the new ecological zone.

Representatives of all major groups of boring bivalves are known to

facultatively bore into shells or other objects lying on the soft

bottoms. Although this represents a straightforward evolutionary step

towards the permanent adaptation to the soft bottoms, the overall

stability of the organism remains rather low. In true soft-bottom

dwellers, boring into small objects is most often seen as being no

more than a juvenile adaptation to increase the overall size and

therefore lessening the risk of accidental disturbances of the life

position. Later in ontogeny, this is complemented or substituted by

more efficient strategies (Savazzi 1982, Chinzei, Savazzi & Seilacher

1982). The calcareous secretion that originarily enabled a few

families of boring bivalves to repair the walls of accidentally

damaged boreholes (Carter 1978; cf. also Massari & Savazzi 1980,

Savazzi 1980) has evolved into calcareous envelopes (crypts; Savazzi

1982c, 1982e) lying freely within soft sediments (tube-dwelling

bivalves; Carter 1978). The coadaptations required by the new life

habit are discussed by Savazzi (1982c; cf. also Carter 1978). The

different adaptations to the tube-dwelling habit are best explained as

the result of convergent evolution. Commensalism with actively moving

soft-bottom corals evolved convergently at least three times in the

r4ytilidae (Savazzi 1982d). The evolutionary pathway that lead to

commensalism in other bivalves (e. g., JousseaumieLLa) is still

unclear.

The adaptive strategies adopted by other sessile bivalves secondarily

adapted to the soft bottoms are discussed by Chinzei 1982, Chinzei,

Savazzi & Seilacher 1982 and Seilacher l982b. Among the secondary

soft-bottom bivalves, representatives of the Pteriomorphia may be

regarded as the least specialized. Several lineages within the Arcidae

never completely lost the capability for active locomotion (Stanley

1970, Thomas 1976, 1978), and often evolved into truly burrowing

Aspects of functionaL morphoLogy 15

secondary forms (e. g., the Anadarinae). A peculiar adaptive shell

morphology featuring a commissure plane twisted into a three-dimensional

s tructure has repeatedly evolved in the pteriomorphiid families Arcidae

(McGhee 1978, Teves z & Carter 1979, Savazzi 198la), Bakevelliidae

(McGhee 1978) and r�ytilidae (Savazzi, manus cript). The adaptive v alue

of this s hell morphology and the underlying morphogenetic mechanisms

are discuss ed in the papers cited above.

It is interesting to note how the method of constructional morphology

allows an explanation of a certain given morphology accounting for the

possibility of parallel evolution and the characteristics of the

BaupLan {the set of basic characters shared by a whole taxon). Since

the conclusions reached for one organism or one group can be checked

against other organisms, they are experimentally testable in a full

scientific sense.

ACKNOWLEOGEI-1ENTS

I thank Richard Reynent for reviewing the present paper and the

manuscript on shell torsion in the �1ytilidae, and Adolf Seilacher for

following and supporting my scientific work in functional morphology

since its very beginning. The research work was financially supported

by the Deuts cher Akademischer Austauschdienst, the Sonderfors chungs­

bereich 53 "Paliikologie" of TUbingen (West Germany), the Exxon

Corporation through the Bermuda Biological Station, and the Swedish

Institute. Institutions that loaned or made available material and

facilities are acknowledged in the separate papers.

1 6 Enrico Savazzi

REFERENCES

Bottjer, D. J. & Carter, J.G. 1 980: Functional and phylogenetic

significance of projecting periostracal structures in the Bivalvia

(Mollusca). Journal of Paleontology 54, 200-216.

Carter, J. G. 1 978: Ecology and evolution of the Gastrochaenacea

(Mollusca, Bivalvia) with notes on the evolution of the endolithic

habitat. Yale Peaboay MUseum Bulletin 41, 92 pp.

Carter, R. M. 1967: The shell ornament of Hysteroconcha and Hecuba

(Bivalvia), a test case for inferential functional morphology.

Veliger 10, 59-71.

Chinzei, K. 1982: Morphological and structural adaptations to soft

substrates in the early Jurassic monomyarians Lithiotis and

Cochlearites. Lethaia 15, 179-197.

Chinzei, K. , Savazzi, E, & Seilacher, A. 1982: Adaptational strategies

of bivalves living as infaunal secondary soft bottom dwellers. In:

Seilacher, A. , Reif, W. -E. & Westphal, F. (eds . ) : Studies in

paleoecology. Neues Jahrbuch fur Geologie und Palaontologie

Abhandlungen 164, 229-244.

Cowen, R. 1979: Functional morphology. In: Fairbridge, R.W. & Jablonski,

D. (eds. ) : The encyclopedia of paleontology, 487-492.

Efremov, !.A. 1940: Taphonomy: new branch of paleontology. Pan­

American Geology ?4, 81-93.

Fisher, D. C. 1977: Functional significance of spines in the

Pennsylvanian horseshoe crab Euproops danae . Paleobiology 3,

175-195.

Frey, E. 1982: Ophisaurus apodus (Lacertil i a, Angui dae) - a stemming

digger? In: Seilacher, A. , Reif, W.-E. & Westphal, F. (eds. ) :

Studies in paleoecology. Neues Jahrbuch fur Geologie und

Palaontologie Abhandlungen 164, 217-221.

Ghiold, J. 1979: Spine morphology and its significance in feeding and

burrowing in the sand dollar, Mellita quinquiesperforata

(Echinodermata: Echinoidea). Bulletin of Marine Sciences 29,

481-490.

Ghiold, J. 1982: Observations on the clypeasteroid Echinocyamus

Aspects of functional rnoPphology 17

pusiZlus (0. F. MUll er). Journal of Experimental Marine Biology

and Ecology 61, 57-74.

Ghiold, J. & Seilacher, A. 1982: Burrowing and feeding in sand dollars

as reflected by the functional differentiations of external

structures. In: Seilacher, A. , Reif, W. -E. & Westphal, F. (eds. ) :

Studies i n paleoecology. Neues Jahrbuch fiir Geologie und

Palaontologie Abhandlungen 164, 221-228.

Gould, S.J. & Lewontin, R. C. 1979: The spandrels of San Marco and the

Panglossian paradigm: a critique of the adaptationist programme.

In: Maynard Smith, J. & Holliday, R. (eds.) : The evolution of

adaptation by natural selection. Proceedings of the Royal Society

of London serie B 205, 581-598.

Hickman, C. S. 1980: Gastropod radulae and the assessment of form in

evol utionary paleontology. Paleobiology 6, 276-294.

Kauffman, E. G. 1969: Form, function and evolution. In: Moore, R. C.

(ed. ) : Treatise on invertebrate paleontology Nl, 129-205.

Kl aassen, F. 1973: Stridulation und Kommunikation durch Substratschall

bei Gecarcinus lateralis (Crustacea Decapoda) . Journal of

Comparative Physiology 83, 73-79.

Kleemann, K. H. 1980: Boring bivalves and their host corals from the

Great Barrier Reef. Journal of Molluscan Studies 46, 13-54.

Lewontin, R. C. 1978: Adaptation. Scientific American 239, 213-230.

Massari, F. & Savazzi, E. 1980: Driftwood transportation of exotic

pebbles in the Upper Cretaceous Scaglia Rossa veneta (Mt. Loffa,

Southern Alps) suggested by teredinid tubes. Neues Jahrbuch fur

Geologie und Palaontologie Monatshefte 1981, 311-320.

McGhee, G. R. Jr. 1978: Analysis of the shell torsion phenomenon in th e

Bivalvia. Lethaia 11, 315-329.

Miller, J. 1975: Structure and function of trilobite terrace lines.

Fossils and Strata 4, 155-178.

Paul, C.R. C. 1975: A reappraisal of the paradigm method of functional

analysis in fossils. Lethaia ?, 15-21.

Pojeta, J. R. & Palmer, T. J. 1976: The origin of rock boring in mytilacean

pelecypods. Alcheringa 1, 167-179.

Purchon, R. D. 1954: A note on the biology of the lamellibranch Rocellaria

(Gastrochaena) cuneiformis Spengler. Proceedings of the Zoological

Society of London 124, 17-33.

18 Enrico Savazzi

Purchon, R.D. 1955: The structure and function of the British

Pholadidae (rock-boring Lamellibranchia). Proceedings of the

ZooLogica� Society of London 124, 859-911.

Raup, D.M. 1972: Approaches to morphological analysis. In: Schopf,

T.J.M. (ed.): ModeZs in pa�eobioZogy, 28-45.

Reif, W.-E. 1975: Lenkende und limitierende Faktoren in der Evolution.

Acta Biotheoretica 24, 136-162.

Reif, W.-E. 1982: Functional morphology on the procrustean bed of the

neutralism-selectionism debate. - Notes on the constructional

morphology approach. In: Seilacher, A., Reif, �J.-E. & Westphal,

F. (eds.): Studies in paleoecology. Neues Jahrbuch fur Geologie

und PalaontoZogie AbhandLungen 164, 46-59.

Rudwick, M.J.S. 1964: The inference of function from structure in

fossils. British. JournaL of Philo sophicaL Sciences 15, 27-40.

Roder, H. 1977: Zur Beziehung zwischen Konstruktion und Substrat bei

mechanisch bohrenden Bohrmuscheln (Pholadidae, Teredinidae).

Senckenbergiana Maritima 9, 105-213:

Savazzi, E. 1980: NPw records of fossil Gastrochaenacea (Pelecypoda)

from the Venetian region (NE Italy). Memorie di Scienze Geologiche

34, 177-182.

Savazzi, E. 198la: Barbatia mytiloides and the evolution of shell

tarsi on in arci d pe lecypods. Lethaia 14, 143-150.

Savazzi, E. 1981b: Functional morphology of the cuticular terraces in

Ranina (Lophoraninaj (brachyuran decapods; Eocene of NE Italy).

Neues ,Tahr·buch fur Geol.ogie und PaUiontologie Abhandl ungen 162,

231-243.

Savazzi, E. 1982a: Shell sculpture and burrowing in the bivalves

Scapharca inaequivalvis and Acanthocardia tul;ercuZata. Stuttgarter

3eitroage zur NatUl'kunde serie A (Biologie) 353, 12 pp.

Savazzi, E. 1982b: Burrowing habits and cuticular sculptures in Recent

sand-dwelling bt·achyuran decapods from the Northern Adriatic Sea

(Mediterranean). New-.• Jahrbuch fu1' Geol.ogie und PaWontolog1:e

. '1l�.!:>:v.3Zungen 16 3, 369-388.

Savazzi, E. l982c: Adaptdtions to tJbt dwelling in the Bi·1alvia.

i.,ethda. I;;, 275-297.

Savazzi, E. 1982d: Commensalism between a boring mytilid bivalve and

a soft bottom coral in the Upper Eocene of northern Italy.

Aspects of functiona� morphoLogy 19

PaLaontoLogisehe Zeitschrift 56, 165-175.

Savazzi, E. 1982e: Clavage1lacea (Bivalvia) from the Venetian region,

NE Italy. Aeta Geo[ogiea PoLonica 32, 83-92.

Savazzi, E. (MS): Adaptive significance of shell torsion in mytil id

bivalves. (Submitted for pubLieation).

Savazzi, E. , Jefferies, R.P.S. & Signor, P.W.lll 1982: Modifications of

the paradigm for burrowing ribs in various gastropods, crustaceans

and calcichordates. In: Seilacher, A. , Reif, W. -E. & l<estphal, F.

(eds.): Studies in paleoecology. Neues Jahrbuch fur GeoLogie und

PaLaontologie Abhandlungen 164, 206-217.

Schmalfuss, H. 1975: Morphologie, Funktion und Evolution der

Tergithocker bei Landisopoden (Oniscoidea, Isopoda, Crustacea).

Zoomorphologie 80, 287-316.

Schmalfuss, H. 1976a: Okologisch-funktionsmorphologisch Untersuchungen

an Karibischen Krabben (Decapoda, Brachyura). I. Percnon gibbesi

(H. Milne-Edwards, 1837) (Grapsidae, Plagusiinae). Studies on the

Neotropical Fauna and Environment 11, 211 - 222.

Schmalfuss, H. 1976b: Panzerskulpturen bei Arthropoden. ZentraZblatt

fur GeoZogie und PalaontoLogie E 1976, 315-316.

Schma1fuss, H. 1977: Morpho1ogie und Funktion der terga1en Langsrippen

bei Landisopoden (Oniscoidea, Isopoda, Crustacea). Zoomoyophologie

86' 155-16 7.

Schma1fuss, H. 1978a: Structure, patterns and function of cuticular

terraces in Recent and fossil arthropods. I. Decapod crustaceans.

Zoomorphologie 90, 19-40.

Schmalfuss, H. 1978b: Morphology and function of cuticular micro-scales

and corresponding structures in terrestrial isopods (Crustacea,

Isopoda, Oniscoidea). ZoomorphoLogie 91, 263-274.

Schma1fuss, H. 1981: Structure, patterns and function of cuticular

terraces in trilobites. Lethaia 14, 311-341.

Seilacher, A. 1961: Krebse im Brandungssand. Natur und VoLk 91,

257-264.

Seilacher, A. 1970: Arbeitskonzept zur Konstruktions-Morphologie .

Lethaia 3, 393-396.

Sei1acher, A. 1972: Divaricate patterns in pelecypod shells. Lethaia

5, 325-343.

Seilacher, A. 1973: Fabricationa1 noise in adaptive morphology.

20 Enrico Savazzi

Systematic Zoology 22, 451-465.

Seilacher, A. 1976: Terrassenlinien des anomuren Krebses Emerita.

Zent�lblatt fUr Geologie und PaZ�ntoZogie lT 1976, 313-314.

Seilacher, A. 1982a: Introduction: burrowing strategies.In: Seilacher,

A., Reif, W.-E. & Westphal, F. (eds.): Studies in paleoecology.

Neuee Jahrbuch fUr Geologie und PaUiontoZogie Abhandlungen 164,

205-206.

Seilacher, A. 1982b: "Hammer oysters" as secondary soft bottom

dwellers. In: Seilacher, A., Reif, W.-E. & Westphal, F. (eds.):

Studies in paleoecology. Neuee Jahrbuch fUr Geologie und

Palaontologie Abhandlungen 164, 245-250.

Signor, P.W.IIT 1980: Shell sculpture aids burrowing in turritelliform

gastropods. Geological Society of America Abstracts with Programs

12, 522.

Signor, P.W.IIT 1982a: A critical re-evaluation of the paradigm method

of functional inference. In: Seilacher, A., Reif, W.-E. & Westphal,

F. (eds.): Studies in paleoecology. Neues Jahrbuch fUr Geologie

und Palaontologie Abhandl ungen 164, 53-63.

Signor, P.W.IIT 1982b: Constructional morphology of gastropod ratchet

sculpture. Neues Jahrbuch fUr Geologie und Palaontologie

Abhandlungen 163, 349-368.

Stanley, S.M. 1968: Post-Paleozoic adaptive radiation of infaunal

bivalve molluscs: a consequence of mantle fusion and siphon

formation. Journal of Paleontology 42, 214-229.

Stanley, S.M. 1969: Bivalve mollusk burrowing aided by discordant

shell ornamentation. Science 166, 634-635.

Stanley, S.t�. 1970: Relation of shell form to life habits in the

Bivalvia (Mollusca). Geological Society of America Memoirs 125,

296 pp.

Stanley, S.M. 1972: Functional morphology and evolution of byssally

attached bivalve mollusks. Journal of Paleontology 46, 165-212.

Stanley, S.M. 1975: Why'clams have the shape they have: an experimental

analysis of burrowing. PaZeobioZogy 1, 48-58.

Stanley, S.M. 1977: ·coadaptation in the Trigoniidae, a remarkable

family of burrowing bivalves. Palaeontology 20, 869-899.

Stanley, S.M. 1981: Infaunal survival: alternative functions of shell

ornamentation in the Bivalvia (Mollusca). Paleobiology 7, 384-393.

Aspects of functional mo:rphology 2 1

Tevesz, M.J.S. & Carter, J.G. 1979: Form and function in Trisidos

(Bivalvia) and a comparison with other burrowing arcoids.

Malacologia 19, 77-85.

Thayer, C.W. & Steele-Petrovic, H.M. 1975: Burrowing of the lingulid

brachiopod Glottidia pyramidata: its ecologic and paleoecologic

significance. Lethaia 8, 209-221.

Thomas, R.D.K. 1976: Constraints of ligament growth, form and evolution

in the Arcoida (Mollusca: Bivalvia). Paleobiology 2, 64-83.

Thomas, R.D.K. 1978: Shell form and the ecological range of living and

extinct Arcoida. Paleobiology 4, 181-194.

Trueman, E.R. & Ansell, A.D. 1969: The mechanisms of burrowing into

soft substrata by marine animals. Oceanography and Marine Biology

Annals Rev. 7, 315-366.

Yonge, C.M. 1955: Adaptation to rock boring in BotuZa and Lithophaga

(Lamellibranchia, Mytilidae) with a discussion on the evolution

of this habit. Quarterly Journal of Microscopical Science 96,

383-410.