LARVAL BIOLOGY OF EARLY CAMBRIAN MOLLUSCS

BULLETIN OF MARINE SCIENCE, 39(2): 536-549, 1986 LARVAL INVERTEBRATE WORKSHOP

LARVAL BIOLOGY OF EARLY CAMBRIAN MOLLUSCS: THE IMPLICATIONS OF SMALL BODY SIZE Chef Chaffee and David R. Lindberg ABSTRACT Current theory suggests that the ancestral larval condition in molluscs was planktic and planktotrophic. Using Recent marine gastropods with similar shell morphologies and Recent molluscan life-history data, we constructed a model that estimates Cambrian univalve fecundities over a range of shell lengths, egg sizes, and body plans. Using the correlation between fecundity and mode of larval development present in Recent marine benthic invertebrates, we infer mode of larval development for Cambrian species. Because of their minute body size, the potential fecundities of most Early Cambrian taxa are substantially below the fecundities correlated with planktic development in Recent gastropods. By the Late Cambrian and Early Ordovician molluscan body size sufficiently increased to produce fecundities similar to those correlated with planktic development in Recent taxa. The life-history patterns present

in extant molluscan groups with Cambrian originations also strongly suggest external fertilization, relatively large eggs and lecithotrophic development as the ancestral condition. We propose that the evolution of larval development in Cambrian molluscs proceeded from nonplanktic lecithotrophic development to planktic lecithotrophic development and that planktotrophic larvae are secondarily derived.

Patterns of larval development in marine invertebrates have been used to address questions of phylogeny (Verrill, 1896; MacBride, 1906; Garstang, 1951; Hyman, 1955; Fell, 1967; Jagersten, 1972; Zimmer, 1973), biogeography (Scheltema, 1971; 1975; 1977; Hansen, 1980; Rex and Waren, 1982; Lutz et al., 1984), ecology (Thorson, 1950; Mileikovsky, 1971; Grahame, 1977; Perron, 1981), and life-history evolution (Vance, 1973a; 1973b; Chia, 1974; Underwood, 1974; Strathmann, 1977; 1978; Stearns, 1977; Christiansen and Fenchel, 1979). In the Mollusca much of this interest has focused on the origin and evolution of feeding larvae. Jagersten (1972), Strathmann (1978) and others have argued that the ancestral larval form was planktic and planktotrophic based on the comparative morphologies of their ciliated band feeding mechanisms. In contrast, Chanley (1968), Salvini-Plawan (1969), and Bandel (1983) have argued for planktic lecithotrophic larvae because of the presence of nonfeeding larvae in all molluscan classes. The one trait that proponents of both scenarios agree on is that the ancestral larva was at least planktic. Until recently, patterns oflarval development were studied almost exclusively by biologists examining Recent species. Now, paleontologists as well as biologists are examining the data present in the fossil record. Paleontologists have recognized that the morphological characters that are correlated with specific larval types or life-history traits in Recent invertebrate species are also present in many fossil taxa (Jablonski and Lutz, 1983). This observation has led workers to infer similar life-history traits for extinct species (mostly molluscs) and has allowed them to recognize and document patterns in the fossil record (LaBarbera, 1974; Shuto, 1974; Hansen, 1978; Jablonski and Lutz, 1980; 1983). The morphological characters most commonly preserved in fossil molluscs, and therefore studied, are the shape and size of the early shell which correlate with feeding versus nonfeeding larval development (Jablonski and Lutz, 1980). These studies have documented changes from feeding to nonfeeding larvae in certain Meso- and Neogastropod 536

CHAFFEE AND LINDBERG: LARVAL BIOLOGY OF EARLY CAMBRIAN MOLLUSCS

537

groups; however, workers have not been able to distinguish between planktic forms and non planktic forms with nonfeeding larvae. Biologists have used the fossil record to estimate times of origin of different larval types. Comparative morphologies of Recent molluscan larvae are used to suggest phylogenetic relationships between living taxa and to infer larval traits at the common ancestor. The fossil record is then examined to establish a minimum estimate of the time of origin of specific larval types (Strathmann, 1978). The importance of scale is easily overlooked when workers combine fossil and Recent data sets to construct evolutionary scenarios, but scale is of particular importance when the earliest molluscs are considered because they were so small (Nicol, 1966 and references therein). Runnegar and Jell (1976) first quantified the minute size of the earliest molluscs. Later, Runnegar (1983) increased the size of the data set and provided finer resolution of the molluscan record through the Cambrian. Runnegar (1983, p. 139) concluded that "most shelled molluscs remained small until the end of the Cambrian" (small refers to a maximum size of < 10 mm and for much of this period 540 million years old). We do this by combining data on the gonad size and egg size in Recent species with Runnegar's (1983) data set on the size of Paleozoic molluscs. We then estimate fecundities for the different shapes of Cambrian univalves. These estimates are then appraised in light of the association between modes of larval development, fecundity and adult size in Recent organisms (Thorson, 1950; Strathmann and Strathmann, 1982) and are used to examine the assertion that the larvae of the earliest molluscs were planktic. MATERIALS

AND METHODS

To estimate the potential fecundities of early Cambrian univalve molluscs we determined: (I) the size range of the Cambrian taxa, (2) their shapes, and (3) calculated the volumes of their shells using the information from 1 and 2. Because of the preservational quality of Cambrian fossils, it was not possible to determine volumes and ultimately potential fecundities from the fossils directly. Therefore, we had to model the Cambrian univalves using the shells of Recent molluscan species with, what we have determined to be, similar shapes. We used the maximum sizes of 157 species of Cambrian molluscs that were recently published by Runnegar (1983) (Fig. I) to establish the size range of the Cambrian taxa. Shapes of Cambrian molluscs are more conservative than Recent species. Pojeta and Runnegar (1976) have proposed that the variation seen in Cambrian univalves can be adequately represented by seven general shell shapes. We matched six of the seven shell shapes by visual examination with similarly shaped shells of both Cambrian molluscs and Recent gastropod species (Fig. 2, Table I). We were unsuccessful in matching Pojeta's and Runnegar's (1976) figure 7D with a Recent species. For each Recent species we calculated the allometric relationship between length and height (except for Trimuscu/us reticu/atus for which we used length and width). Each specimen of a Recent species was chosen on two criteria: (I) those individuals that best fit the general Cambrian shell form that they were supposed to represent, and (2) those individuals that extended the range of sizes for a given shape. We measured three dimensions of each individual: greatest shell length, width and height. For each species of Cambrian mollusc, similar measurements were taken from illustrations in monographs of Cambrian fauna (Raaben, 1969; Runnegar and Jell, 1976; Pojeta and Runnegar, 1976; Runnegar, 1983). As many illustrations of different individuals as possible were measured for each species.

538

BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2, 1986

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Shell volumes were measured with one of two methods. Larger shells were placed apex down in clay with the anterior-posterior plane horizontal. The shell was then filled with distilled water from a calibrated syringe until the meniscus was even with the shell margin; the syringe was calibrated to the nearest 0.01 cc. This method was only used on shells with volumes greater than 0.03 cc so the measurement error would not exceed the precision of the syringe. Shells with smaller volumes required a second method of measurement. Each small shell was placed in clay, apex down, margin horizontal. We then weighed each shell-clay set both before and after filling the shell with distilled water. The empty and full shells were weighed to the nearest 0.000 I g. Repeated weighings of the same shells yielded a measurement error of less than 2%. The weight of the water was converted to volume using the conversion factor, I g = Icc. The allometric change in dimensions was determined for all Recent and fossil species. This was done by using least squares regressions on logarithmically transformed data. Even though both variables


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BULLETIN OF MARINE SCIENCE, VOL. 39, NO.2,

1986

Table I. Regression statistics ofIength (L) vs. height (H) and length (L) vs. volume (V) for Cambrian and Recent species X

System/Taxon

Cambrian A. Ginella savitskii

L L L L L L L L L L L L

B. Bennella jacutica C. 19orella ungulata E. Tannuella elata F. Mellopegma georginensis G. Vallototheca spp. Quaternary A. Puncturella cooperi

L L L L L L L L L L L L

B. Crepidula adunca C. Hipponix tumens E. Crucibulum sp. F. Phenacolepus sp. G. Trimusculus reticulatus

Y

H V

H V

H V

H V

H V

H V

H V

H V

H V

H V

H V

H V

Y-int.

Slope

0.460 0.047 (10-4) 0.750 0.0937 0.623 0.122 0.780 0.213 0.520 0.0012 1.000 0.316

1.00 3.00 1.00 3.00 1.00 3.00 1.00 3.00 1.00 3.00 1.00 3.00

0.870 0.250 0.450 0.096 0.572 0.159 2.120 0.730 0.254 0.139 1.223 0.413

1.007 2.450 1.024 3.001 1.048 2.848 0.622 2.533 1.026 2.827 0.518 2.354

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0.750 0.840 0.950 0.960 0.900 0.950 0.614 0.950 0.900 0.970 0.437 0.910

** ** ** ** ** ** ** ** ** ** ** **

contained error terms, we used a regression solution in preference to the major axis and reduced major axis methods, because our analyses were used for both predictive and descriptive purposes (Sokal and Rohlf, 1981 for statistical implications). In all cases length was used as the predictor for volume. This was not because it consistently had the highest correlation coefficient, but because it was the single measurement that was available for all Cambrian and Recent species. To determine at which size and shape the Recent species best matched its fossil counterpart, we plotted the allometric curves ofthe Recent mollusc species against the isometric curves of the Cam brian species for each of the six general shell forms. The isometric curve for each fossil species was generated by taking the mean values for length and height or length and width from the measurements and plotting a line with a slope of 1.0 through this value. This line represents a constant shell shape over a range of sizes. The point of intersection between the allometric and the isometric curves for each shell form was then used as the point where the two Recent and Cambrian species were equal in size and shape. The number of eggs (fecundity) produced by any given shell shape at any given size was calculated as follows: Fecundity

=

% gonad x shell volume/egg volume.

The proportion of shell volume occupied by gonad and the size of the eggs produced in Cambrian species are unknown. For estimates of fecundity gonad volume was set at 25% and 50% of the total internal shell volume. For comparative purposes, estimates of gonad size in extant "primitive" molluscs such as aplacophorans, monoplacophorans and polyplacophorans were obtained from Hadfield (1979) and Pearse (1979) and by reconstructing the volume of the gonad of the extant monoplacophoran Neopilina galatheae from serial sections and reconstructions illustrated in Lemche and Wingstrand (1959). Egg sizes between 60 !Lmand 250 !LIDwere used because these sizes correspond to the range of egg

541


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