direction to that of Hoernesia and the other twisted bakevelliids. Field observations con firm the semi-infaunal pleurothetic life habit predicted from the shell ...
Palaeogeography, Palaeoclimatology, Palaeoecology, 46 (1984): 313-324
313
Elsevier Science Publishers B.V. , Amsterdam- Printed in The Netherlands
FUNCTIONAL MORPHOLOGY AND AUTECOLOGY OF PSEUDOPTERA (BAKEVELLIID BIVALVES, UPPER CRETACEOUS OF PORTUGAL)
IU S UNES 0 I
ENRICO SA VAZZI Paleo ntologiska Institutio nen, Box 558, S-75122 Uppsala (Sweden)
Project MID-CRETACEOUS EVENTS
(Received December 2, 1983; revised version accepted March 13, 1984)
ABSTRACT Savazzi, E., 1984. Functional morphology and autecology of Pseudoptera (bakevelliid bivalves, Upper Cretaceous of Portugal). Palaeogeogr., PalaeoclimatoL, PalaeoecoL, 46: 313-324. Pseudoptera sp. nov. is sinistrally twisted about the hinge axis, i.e., in the opposite direction to that of Hoernesia and the other twisted bakevelliids. Field observations con firm the semi-infaunal pleurothetic life habit predicted from the shell morphology. The twisted Bakevelliidae are unlikely to have evolved from soft-bottom forms. A transition from an epibyssate habit on solid substrates to an endobyssate, semi-infaunal life habit probably triggered the evolution of shell torsion in this family, as in the Arcidae and Mytilidae.
INTRODUCTION
Twisted bivalves are characterized by a torsion of the commissure plane along the hinge axis. Shell torsion has been described in the Arcidae (McGhee, 1978; Tevesz and Carter, 1979; Savazzi, 1981), Bakevelliidae (McGhee, 1978; Seilacher, 1984), and Mytilidae (Savazzi, 1983, 1984). Some Buchiidae possess a non-planar commissure comparable with that of twisted bivalves, but the adaptive value of this feature has not been investigated (A. Seilacher, pers. commun., 1983). In all the studied cases, shell torsion is associated with a semi-infaunal, endobyssate life habit and a pleurothetic life position (Fig.1). The twisted shell morphology is functional in several respects: (a) The byssal region of the commissure is carried at a greater depth within the sediment, thus providing a firmer anchorage by the byssus. Present address: Department of Paleobiology, Smithsonian Institution, Washington, DC 20560 (U.S.A.). 0031-0182/84/$03.00
© 1984 Elsevier Science Publishers B.V.
314
Hoernesia (BAKEVELLIIDAE)
Fig.l. Reconstruction of the twisted bakevelliid Hoernesia socialis ( Schlotheim ) from the Middle Triassic of Federal Germany, in life position within a soft sediment.
(b) The posterior region of the commissure emerges from the sediment in an inclined or horizontal position. This orientation reduces the vulnerability of the exposed commissure to accidental damage. At the same time, a considerable length of the commissure is left exposed above the surface of the substrate, allowing the inhalant and exhalant mantle regions to be widely separated (significantly, shell torsion is known only in bivalves devoid of siphons and possessing relatively inefficient, unspecialized gills). (c) the weight of the posterior region of the shell is distributed on a wider surface, which reduces the risk of sinking into a soft substrate. In the twisted bakevelliid
Hoernesia,
the left valve, which lies lowermost
in the life position, is consistently thicker than the right one. The resulting displacement of the center of gravity, together with the general shell shape, favours the passive re-orientation of the shell by waves and water currents (McGhee,
1978).
The direction of twisting in the Arcidae and Bakevelliidae is a constant character at the generic or specific level, and appears therefore to be genetic ally fixed. Within the Arcidae,
Trisidos is always sinistrally twisted (McGhee, whileBarbatia mytiloides is dextrally twisted (Savazzi, 1981). Other species of Barbatia are possibly sinistrally twisted. The twisted bakevelliids studied by McGhee (1978) and Seilacher (1984) are
1978;
Tevesz and Carter, 1979),
dextrally twisted. Several species of the mytilid
Modiolus
facultatively display the shell
twisting phenomenon, although to a lesser extent than the two preceding families (Savazzi,
1983, 1984).
In all the twisted species of Modiolus studied
by the writer, both sinistral and dextral torsion occurs with the same statist ical frequency. In this genus, the direction of shell torsion is most likely a phenotypic character related to the shell orientation within the substrate. Observations on living
Modiolus americanus
in. its natural environment in
Bermuda showed an almost perfect correspondence between the life position and the direction of shell torsion (Savazzi,
1983, 1984).
In the Mytilidae, the limited degree of shell torsion and the absence of other inequivalve characters probably facilitated the evolution of the eco-
315
phenotypic development of the torsional direction. In the twisted Arcidae and Bakevelliidae, on the other hand, the fixed direction of shell torsion is accompanied by other genetically determined inequivalve characters, inherited by non-twisted ancestors. While inequivalve characters (other than shell torsion) in the Arcidae are rather inconspicuous (cf. McGhee,
1978;
Savazzi,
1981),
in the bakevelliid
stock the left valve is often significantly more convex and strongly sculptured than the right one. These inequivalve characters persist in the twisted repre sentatives, and have been interpreted as functional features related to the pleurothetic life habit (i.e., with the commissure not perpendicular to the surface of the sediment in the life position) (McGhee,
1978;
Seilacher,
1984).
The present paper originated from the discovery that the bakevelliid
Pseudoptera
sp. nov. from the Upper Cretaceous of Portugal is sinistrally
twisted, i.e., in the opposite direction to that of the other twisted Bakevel liidae. This suggests that the life position of
Pseudoptera
was also inverted
with respect to
and the other twisted genera. Thus, the inequivalve
characters
cannot have the same adaptive value as in the other
Hoernesia Pseudoptera in
forms. Although the following discussion is based exclusively on the material from
Portugal,
other species of
Pseudoptera
illustrated in the literature
appear similar enough to suggest that the conclusions reached in this paper apply to the whole genus. The question arises whether the evolution of opposite directions of torsion within the Bakevelliidae represents a random "choice" of the non-twisted ancestors, as hypothesized for the Arcidae (Savazzi,
1981),
or was rather
channeled by different preadaptations. ·MATERIAL AND METHODS
Specimens of
Pseudoptera
sp. nov. were collected for this study from the
Lower Cenomanian (Cretaceous) deposits along the coast between Praia da Baforeira and Praia de Carcavelos, approximately Portugal (see Berthou and Lauverjat,
1979).
20
km west of Lisbon,
Specimens exposed by weather
ing were photographed before extraction, to record the shell orientation within the sediment. As a whole, about
30
specimens were collected or
observed in the field. Collecting took place as part of a field course by a team from the Department of Historical Geology and Palaeontology of the Uppsala University. The material illustrated in the present paper is stored in the collections of the above-mentioned institution. TAXONOMY
The specimens used for the present study show rather close affinities with
Pseudoptera anomala
(Sowerby) from the Lower Cretaceous (Aptian) of
England. A preliminary investigation suggests that the material from Portugal belongs to an undescribed species. A review of the whole genus, necessary to solve the taxonomic problem, lies beyond the scope of the present paper.
316 PALAEOECOLOGY
The sediments indicate a low-energy, very shallow water basin or tidal flat during a regressive phase (Berthou and Lauverjat, data). Most of the specimens of
Pseudoptera
1979;
Savazzi, unpublished
were collected from sandstones
with a variable content of CaC03, but the occurrence of the species, and of the other macrofossils as well, does not seem to be related to a particular lithofacies. The associated macrofossils are mostly oysters, infaunal bivalves and gastropods. Bivalve shells are often complete and closed, but only the larger specimens are usually found in life position. The presence of clusters of
Crassostrea
specimens growing vertically on
top of each other ("relais growth"; cf. Chinzei et al.,
1982;
Chinzei,
198 2)
suggests a very high rate of sedimentation. The sediment type and faunal association are often very different from bed to bed, suggesting rapid changes in the
environmental conditions. Further palaeoecological analysis must
await a more detailed study. SHELL MORPHOLOGY AND GROWTH
Shell torsion in
Pseudoptera
sp. nov. reaches or exceeds
90°
between the
byssal and the posterior shell regions. This degree of twisting is higher than that observed by McGhee
(1978)
in the bakevelliid
° Hoernesia (35°-45 ),
and is comparable with that of the more highly twisted species of the arcid genus
Trisidos (80° -90° ).
The shell is longitudinally elongated, triangular, with beaks at the anterior extremity. The hinge line lies at an angle with the major shell axis, forming a pterioid wing running for about three-quarters of the shell length. The liga ment is multivincular, with
4-5
ligamenta! pits in the adults. The hinge
structure was not observed. A narrow byssal gape is present in the antero ventral part of the commissure. Regardless of the lateral asymmetry resulting from shell torsion,
tera
Pseudop
is highly inequivalve. The left valve bears two prominent ridges running
from the umbo to the posterior margin. The ventral ridge separates the postero-lateral and ventral shell regions, which are folded at
90°
to each
other. This folding preceded in ontogeny the development of shell torsion (Fig.3). Therefore, in the juveniles the byssus already emerged from the shell directed towards the right side, suggesting a pleurothetic life position since early stages. Shell torsion subsequently enhanced the lateral displacement of the byssal region by moving it towards the right side. This contrasts with the situation in the other twisted bivalves, in which the byssus emerges in a ventral direction in the juveniles. The left valve bears a radial sculptural pattern, while the right valve shows only faint growth lines. Shell growth took place in two distinct phases: in the first, the shell approached the adult size, while remaining uniformly thin. In the second phase, the shell margins essentially stopped growing, except at the posterior
317
Fig.2. Pseudoptera sp. nov. from the Lower Cenomanian (Cretaceous) of Portugal. A-D. Left lateral, right lateral, dorsal and ventral views of adult specimen with disarticulated valves, X 0.66. E. Juveniie specimen, X 0. 7 5. Note a small oyster attached near the hinge (top left), and worm tubes near the postero·ventral commissure (at bottom). F. Posterior region of adult specimen with two bivalve boreholes, X 0.66. G. Anterior region of adult specimen, X 0.66. H. Internal side of right valve, X 0.66.
319
Fig.4. Field photographs of specimens of Pseudoptera sp. nov. in life position within the sediment, exposed by weathering. Scale is 1 cm in all photographs. A. Juvenile specimen exposed on bedding plane.
B. Transversal section of the anterior region of a shell, perpen
dicular to the bedding plane. Note the byssal part of the commissure lying lowermost, and an oyster cemented to the left valve (uppermost). C. Oblique section of the posterior region of shell, parallel to the bedding plane.
This life position is further confirmed by field observations on specimens exposed by weathering. With very few exceptions, complete individuals with closed valves occur in the hypothesized life position (Fig.4). The distribution of epibionts and borers further confirms the hypothesized life position (Fig.2). It is interesting to note that small oysters are sometimes found attached on the anterior part of the left (uppermost) valve of juvenile
Pseudoptera. Settlement of these epibionts likely took place during the epi faunal life stage. Boring bivalves are found only in adult, thick-shelled indivi duals, and their position is consistent with a semi-infaunal life habit. The pattern of repaired breakage of the shell margin, resulting from the accidental impact of objects rolled on the bottom by waves or currents, is
320
Fig.5. Reconstruction of an adult individual of Pseudoptera sp. nov. in life position. The arrows indicate the direction of the respiratory currents. A. Lateral view. B. View from above, showing the exposed shell regions.
also significant. As in other semi-infaunal bivalves, breakage is concentrated to the posterior, exposed shell region. Life on muddy substrates requires particular adaptations (see Thayer,
1975).
The low shear strength and density of these sediments, in particular,
prevent the adoption of a heavy shell as stabilization against disturbances of the life position (cf. Seilacher,
1984).
In order to avoid sinking into soft sedi
ments, the organism must have a bulk density comparable with that of the substrate, and distribute its weight on a wide surface. The ostreid
Gryphaea
is an exception to this rule, since early species are often thick-shelled and highly convex. These characters are adaptations favouring passive re-orienta tion in high-energy environments (Seilacher, in press). Several lineages of this genus have subsequently evolved towards flatter, larger and comparatively lighter forms (Hallam,
1968).
The ontogenetic changes in shell shape and thickness (Fig.3) suggest a change in life habits during growth. While the light and streamlined shell of the juveniles is better suited to an epifaunal or semi-infaunal life habit with
321
most of the shell exposed at the surface of the sediment, the massive adults with conspicuous sinuses in the posterior region, such as the one in Fig. 5, were probably mostly buried in the sediment. This change in life habits would have solved some of the problems assoc iated with sessile life on muddy substrates. In these environments, juveniles are especially vulnerable to sinking into the sediment. The juveniles of
Pseudoptera,
being light-shelled, were less likely to sink, while the byssus
alone constituted a sufficient anchorage in low-energy environments. The juvenile shell shape with a convex left (uppermost) valve and a flatter right valve probably also facilitated the passive re-orientation by water move ments (by the same mechanism with which waves orient shells on a beach with the convex side upwards) and, in the life position, reduced drag by water currents. Thus, passive re-orientation may have been obtained without the increase in weight connected with differential valve thickening. During growth, sinking of the shell into the substrate and sedimentation would lead to a semi-infaunal life habit. Adults, in virtue of their sheer size, were less vulnerable to fouling caused by sinking into the mud. In addition, weighting of the anterior region of the shell by secondary thickening ensured that this region would tend to lie lowermost, so that the posterior shell margin remained pointed upwards. The flat pinniform shell, rather than sink ing in a horizontal position, would tend to slice its way obliquely in an anterior direction, with the heavy beaks lowermost. Since the beaks are at the anterior extremity of the shell, growth took place essentially in the posterior direction, thus contributing towards main taining the posterior commissure above the surface of the sediment. The inequivalve shell sculpture, being developed only on the left (upper most) valve, may have been functional in reducing erosional scour around the exposed shell regions (cf. Bottjer and Carter,
1980).
Periostracal projec
tions may have increased the roughness of the surface. In the twisted arcid
Trisidos bellunensis,
a similar sculptural pattern has been interpreted as a
burrowing sculpture (Savazzi,
1981).
Since the Bakevelliidae probably were
not active burrowers, this explanation is not applicable to Pseudoptera. In other twisted Bakevelliidae, the sculpture on the left valve (which was lowermost, because of the opposite direction of torsion) was interpreted as a frictional anchor supplementing the byssus (McGhee,
1978).
Since the sculp
ture in most Bakevelliidae (including non-twisted forms) is stronger on the left valve, this character can be regarded as part of the group's "Bauplan" (the set of recurrent characters common to a taxon). While these characters were indeed susceptible to morphological adaptation as a result of selective pressure, their genetic and morphogenetic programming was apparently too rigid to allow more substantial changes like lateral inversion. DISCUSSION
In the above section, it has been shown that the functional significance of shell torsion in
Pseudoptera
and in the other twisted bivalves is roughly the
322
same, but the adaptive strategies as a whole differ. The opposite direction of torsion of Pseudoptera with respect to
Hoernesia
and the other twisted bake
velliids suggests that the evolution of shell torsion took place independently in these genera. Similar conclusions have been reached for the arcids and
Barbatia mytiloides,
Ttisidos
which also display opposite torsion directions and
distinct adaptive strategies (Savazzi, 1981). Secondary shell thickening in ficance than in
Hoernesia.
Pseudoptera
has a different functional signi
While in this last genus the different thickness of
the valves was an adaptation to favour passive re-orientation, shell thickening in
Pseudoptera
appears to have been functional in displacing the center of
gravity toward the beaks, and was related to a change in life habits during ontogeny. In the twisted bakevelliids studied by McGhee (1978) and Seilacher (1984), the more convex left valve may be interpreted as an adaptation to keep the mantle margin above the sediment-water interface (like, for instance, in many oysters). In these forms, reclining on the left valve was probably more advantageous, since it allowed exploiting the already existing difference in valve convexity. A life position with the flat right valve resting against the substrate, on the other hand, may be consistent with an ebibyssate habit in which the shell reclines against the substrate instead of being perpendicular to it. Such a life habit, which represents a conceivable evolutionary pathway from hypothet ical epibyssate forms to
Pseudoptera
sp. nov., may have been adopted also
by juveniles of this last species. It is remarkable that the peculiar shell shape of
Pseudoptera
allowed emergence of the byssus at a right angle with respect
to the posterior commissure already in the earliest growth stages, i.e., before the ontogenetic onset of torsion (Fig.3). While the twisted Arcidae and Mytilidae evolved from hard-bottom epi byssate forms that secondarily returned to the soft bottoms (McGhee, 1978; Savazzi, 1981, 1983, 1984), the twisted Bakevelliidae are believed to have evolved from soft-bottom ancestors ( Stanley, 1972; McGhee, 1978). This would imply that the evolutionary pathways leading to the same basic morphology were altogether different in these families. An analysis of the evolutionary patterns of adaptive strategies in the hi valves shows that major changes are almost invariably triggered by a change of habitat (usually, from soft bottoms to hard bottoms or vice versa: Savazzi, 1981, 1982, 1983, 1984; Chinzei et al., 1982; Seilacher, 1982b, 1984; and references herein). In the specific case of the Bakevelliidae, it is difficult to conceive such a profound change in the morphogenetic programme as shell torsion, without an accompanying major change in habitat. By analogy with the other twisted bivalves, one would expect the ancestors of the twisted bakevelliids to have been epibyssate forms attached to solid substrates, rather than semi-endo byssate soft-bottom dwellers. As in the Arcidae, it may be supposed that these ancestors were byssally attached to solid objects lying on the soft bottoms and resting on the sediment
323
surface, reclining on one side. The inclined commissure reduced both drag by water currents and vulnerability of the shell margins to wear and acciden tal damage (see also Savazzi, 1981, 1984). The anchoring action of the byssus was supplemented by the weight of the shell resting directly on the substrate. Contrary to the ideas of Stanley (1972), Seilacher (1984) suggested that the Bakevelliidae did not evolve from primary soft-bottom dwellers. More over, some Mesozoic Bakevelliidae were certainly epibyssate on solid sub strates (e.g.,
Gervillia lanceolata
from the Lias of West Germany, epibyssate
on ammonites: Seilacher, 1982a, 1984). Several of these forms are possible ancestors to secondary soft-bottom dwellers. Until the evolution within the Bakevelliidae is known with better detail, however, no satisfactory hypothesis can be done on the lineages leading to the twisted forms. ACKNOWLEDGEMENTS
R. Reyment and
A.
Seilacher read and commented on preliminary drafts
of this paper. The field work in Portugal was supported through the Institute of
Historical
Geology and Palaeontology,
Uppsala University.
A
Guest
Scholarship by the Swedish Institute is gratefully acknowledged. REFERENCES Berthou, P. Y. and Lauverjat, J., 1979. Essai de synthese paleogeographique et paleobio stratigraphique du bassin accidental portugais au cours du Cretace superieur. Cienc. Terra, 5: 121-144. Bottjer, D. J. and Carter, J. G., 1980. Functional and phylogenetic significance of project ing periostracal structures in the Bivalvia (Mollusca). J. Paleontol., 54: 20o-216. 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. and Seilacher, A., 1982. Adaptational strategies of bivalves living as infaunal secondary soft bottom dwellers. In: A. Seilacher, W.-E. Reif and F. Westphal (Editors), Studies in Paleoecology. Neues Jahrb. Geol. Palaeontol. Abh., 164: 229244. Hallam, A., 1968. Morphology, palaeoecology and evolution of the genus Gryphaea in the British Lias. Philos. Trans. R. Soc. London, Ser. B: 91-128. McGhee Jr., G. R., 1978. Analysis of the shell torsion phenomenon in the Bivalvia. Lethaia, 11: 315-329. Savazzi, E., 1981. Barbatia myti loides and the evolution of shell torsion in arcid pele· cypods. Lethaia, 14: 143-150. Savazzi, E., 1982. Adaptations to tube dwelling in the Bivalvia. Lethaia, 15: 275-297. Savazzi, E., 1983. Aspects of the functional morphology of fossil and living invertebrates (bivalves and decapods). Acta Univ. Ups. Abstr. Uppsala Diss. Sci., 680: 1-21. Savazzi, E., 1984. Adaptive significance of shell torsion in mytilid bivalves. Palaeontology, 27: 307-314. Seilacher, A., 1970. Arbeitsconzept zur Konstruktions·Morphologie. Lethaia, 3: 393-396. Seilacher, A., 1982a. Ammonite shells as habitats in the Posidonia shales of Holzmaden floats or benthic islands? Neues Jahrb. Geol. Palaeontol. Monatsh., 1982: 98-114. Seilacher, A., 1982b. "Hammer oysters" as secondary soft bottom dwellers. In: A. Seilacher, W.·E. Reif and F. Westphal (Editors), Studies in Paleoecology. Neues Jahrb. Geol. Palaeontol. Abh., 164: 245-250.
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Seilacher, A., 1 984. Constructional morphology of pelecypods: evolutionary pathways in primary versus secondary soft bottom dwellers. Palaeontology, in press. Stanley, S. M., 1 972. Functional morphology and evolution of byssally attached bivalve mollusks. J. Paleontol., 46: 165-212. Tevesz, M. J. S. and Carter, J. G., 1979. Form and function in Trisidos (Bivalvia) and a comparison with other burrowing arcoids. Malacologia, 1 9: 77-85. Thayer, C. W., 1 975. Morphologic adaptations of benthic invertebrates to soft substrata. J. Mar. Res., 3 3: 1 77- 1 89.
