the Alexander Fellowship and Palmer Award to MPR. Carole. Hickman, James Valentine, Wayne Sousa, and Peter Rodda commented on earlier drafts of the ...
Experimental taphonomy of embryo preservation in a Cenozoic brooding bivalve MICHAEL P. RUSSELL, JOHN P. HUELSENBECK AND DAVID R. LINDBERG
LETHAIA
Russell, M. P., Huelsenbeck, J. P. & Lindberg, D. R. 1992 10 15: Experimental taphonomy of embryo preservation in a Cenozoic brooding bivalve. Lethaia. VOI. 25. pp. 353-359. O S I ~ISSN . 0024-1164.
To distinguish between alternative explanations for the presence of synchronous broods in the MiocenePliocene bivalve, Transenriello species. we performed in situ burial experiments of the Recent species T. corfzisa. All Recent Transennella species are asynchronous brooders; a single brood contains all or most developmental stages. Specimens from Miocene-Pliocene deposits of California suggest that some members of this taxon were synchronous brooders, i.e.. all the embryos of a brood develop simultaneously with only one developmental stage represented at any time. The presence of synchronous Trunsennella broods in the Miocene-Pliocene could indicate that an evolutionary change in mode of reproduction has occurred in this genus. Alternatively, asynchronous brooding in this taxon may he conservative and preferential preservation of later stages of development, or seasonal variation in reproduction, could result in a taphonomic overprint. Our burial experiments indicate that the earliest stages of development are almost entirely lost; however. there is enough preservation of the later stages of development to distinguish the two modes of reproduction. Additionally. we discovered a single fossil specimen with an asynchronous brood. Based primarily on this specimen, and observations from the burial experiments, we conclude that the fossil synchronous broods are an artifact of preservation and asynchronous brooding in Transeniiella is conservative. TR.(NSENNELLA, taphonomy, Miocene Pliocene, life history. brooding. biostratinomy. -
Michael P. Russell. Department of Biology, Villanotu lJnit~ersi/y,Villanotu, P A i908S, USA; John P. Huelsenbeck, Department of Ceologicol Sciences, Uniwrsity of Texas, Austin, Texas 78713, U S A ; David R. Lbidberg. Mirseum uf Paleonrolog~,Uniiwrsiry of California, Berkeley, California. 94720, U S A ; received 18th September. 1991. rei)i.sed typescript accepted 3rd May, 1992.
Fossilized embryonic stages of the venerid bivalve Traiisennella sp. were first reported by Lindberg ( 1984) from Miocene-Pliocene deposits of the Etchegoin Formation in the Kettleman Hills, California. These well-preserved embryonic stages were found inside articulated adult specimens and establish the presence of the brooding mode of reproduction in this taxon at least as far back as the Pliocene. These specimens also suggested an evolutionary change in the reproductive life history strategy of this taxon sometime between the Miocene-Pliocene and the Recent. Today. two species of Transennella occur along the California coast - Transennella tantilla and T. confiisa. Both species asynchronously brood their developing embryonic and early juvenile stages between the inner demibranch and the visceral mass (see Kabat 1985:274; Gray 1982). Asynchronous, or sequential, brooding occurs when all or most developmental stages are represented in a single clutch. This is in contrast to the synchronous mode of reproduction, where all individuals within a clutch are of the same devel-
opmental stage. The synchronous brooding mode of reproduction is present in other venerid bivalves, e.g., Gemma gemma (Sellmer 1967). The embryonic valves Lindberg (1984) reported from fossilized Miocene-Pliocene Transennella sp. broods were all of the same size, i.e., they all represented the same developmental stage. This suggested th'at an evolutionary change from the synchronous mode of reproduction to the asynchronous mode had occurred some time between the Miocene-Pliocene and the Recent (Lindberg 1984). In brooding species, timing of reproduction and constraints on the packing of developing embryos are critical factors in the evolution of life history features (Chaffee & Strathmann 1984; Strathmann & Chaffee 1984; Chaffee & Lindberg 1986). Documenting a shift in the brooding mode of reproduction in the fossil record holds many exciting possibilities for elucidating the selective forces molding life history evolution. However, before examining these fossil broods in the light of life history theory, alternative taphonomic explanations for the pres-
354
Midiad P. Rttssell and others
ence of synchronous broods in the fossil specimens must be explored. Seasonal variation in reproduction of marine invertebrates is a common phenomenon (Strathmann 1987; Giese et al. 1987 and references therein). Sastry ( 1979) summarizes the seasonality of breeding periods of 87 bivalve species; of these, 20 have known modes of development and 5 of them are direct developers. There are various facets to seasonal variation in reproduction which could affect the relative distribution of developmental stages within the clutch of an asynchronous brooder. Previously, we demonstrated that both levels of fecundity and relative proportions of developmental stages within broods of Transennella confusa vary seasonally (Russell & Huelsenbeck 1989). It is possible that the fossil broods reflect this seasonality rather than an evolutionary shift in life history. For example, during the winter season the broods of T . confusa are dominated by the later stages of development. If a brooding adult was entombed during this phase of the reproductive cycle. then the resulting fossil could give the appearance of the synchronous mode of reproduction. In this situation, the taphonomic overprint due to seasonal variation in reproduction would result in misinterpreting the evolution of life history features in Transennella. A more obvious and potentially misleading source of taphonomic bias in the fossilization of Tronsennellu broods would result from differential preservation of developmental stages within a clutch. As embryonic valves grow they become more heavily calcified and shell mineralogy and elemental composition change during ontogeny (Rosenberg 1980). The interaction of these factors could result in the preferential preservation or loss of discrete size classes of embryos. If certain stages of developing embryonic valves are more likely than others to be preserved in an asynchronous brooder, then the resulting fossilized broods would appear to consist of just one or a few developmental stages. The taphononiic overprint of preferential preservation could lead to the erroneous interpretation that the taxon in question possessed the synchronous mode of development. Moreover, preferential preservation of embryos and seasonal variation in reproduction could occur at the same time to produce the appearance of fossilized synchronous broods from an asynchronous brooder.
LETHAIA 25 f 1992)
Field site
\ I
Fig. 1. Map showing the Pillar Point Harbor study site (37"30'N, 122"28'W) where the burial experiments were performed and the Kettleman Hills Miocene-Pliocene fossil locality, UCMP D-9939 (University of California Museum of Paleontology), where fossil Transennelh sp. broods were found.
To address the issue of taphonomic bias in the preservation of Transennella broods in the fossil record, we studied a Recent population of T . confusa at Pillar Point Harbor, San Mateo County, California (Fig. I). In addition to quantifying seasonal variation in reproduction (Russell & Huelsenbeck 1989) we performed in situ burial experiments at different phases of the reproductive cycle. Furthermore, we re-sampled the original Kettleman hills deposits and report o n additional fossil Transennella broods from this area.
Materials and methods Pillar Point Harbor (37"30'N, 122"28'W, Fig. 1 ) is a small (approximately 2 km2), artificially en-
LETHAIA 25 (1992)
Experimental taphonomy of brooding bivalve
355
closed embayment 32 km south-southwest of San the clams were buried underneath approximately Francisco, California. It is the northern portion 36 cm of sediment). Six tubes were buried on 15 of Half Moon Bay. The area supports a rich May 1987 and six on 18 January 1988. In addiintertidal mudflat community including, e.g., tion, dissections of a subsample of live clams Tresus nuttalli, Polinices lewisi and Oliaella bipli- were performed on these dates to determine origcata. Transennella confusa is the numerically inal levels of fecundity and brood size structure. dominant molluscan species in the area, several To estimate the fossilization potential of the hundred individuals can easily be collected by different stages of development, we counted meascraping off the top 1-2 cm of a small ( < 1 m2) sured individual embryos under cross polarized area of substratum with a shovel and screening light. This technique made the calcified valves of the sediments. Fig. 1 shows the field site where all the developing embryos visually distinct from the the T. confusa examined in this study were col- soft tissue (e.g., Fig. 2). Gallucci and Kawaratani ( 1975) buried lected, it is also the area where the burial experiTransennella tantilla to use as a model for estiments were performed. We documented seasonal variation in two mating juvenile mortality of the commerically components of brooding reproduction in T. con- important littleneck clams, Protothaca staminea fusa: (i) fecundity and (ii) relative proportions of and Venerupis japonica. These mortality data are developmental stages ( Russell & Huelsenbeck important to fisheries managers because it had 1989). Levels of fecundity are lowest in the winter long been suspected that high levels of juvenile and approximately the same throughout the mortality result from the excavation activities of spring, summer and fall. The later stages of de- commerical and recreational clam diggers. They velopment dominate the winter broods, whereas found 91% mortality after 11 days of burial the earliest stages dominate the spring broods under 8 cm of sediment. They did not address the (both summer and fall are intermediate, Russell possibility that T . tantilla might dig its way out & Huelsenbeck 1989293). To assess the effects from underneath the sediments nor were there that initial biodegradation and biostratinomic any differences in their samples between the numprocesses have on the preservation potential of ber of clams recovered from the 8 cm depth and embryonic valves, we performed a series of in situ the surface. Moreover, Armstrong (1965) found burial experiments. We buried live clams during that for 10 additional species of bivalves, burial the phases of the reproductive cycle when the in sediment in excess of 10 to 18 cm was sufficient brood structure differed most, i.e., during the to ensure 100% mortality. We designed the burial winter (low fecundity. highest proportion of large experiments and cages based on the study of embryos) and spring (high fecundity, lowest pro- Gallucci and Kawaratani (1975), assuming that if T. confztlsa had the ability to dig its way towards portion of large embryos). Because of the small size of T. coilfzisa (maxi- the surface, the buried clams would not escape mum length observed in this study is 5.50mm), the 16 cm of sediment covering them in the tubes. Apparently, T. confu:a has the ability to extriwe found it necessary to use burial cages to ensure the subsequent retrieval of buried clams. cate itself from underneath sediments. When the first two tubes from the May 1987 burials were We constructed the cages out of acrylonitrile-butadiene-styrene (ABS) pipes; inside diameter processed, many of the clams were found towards 10.0 cm, outside diameter 11.5 cm, and 20 cm the tops of the tubes. In addition, one of the high. Screen mesh (1 mm) was glued to the bot- tubes buried for eight months only retained 4 out tom, but the tops were left open. The bottom of the 40 clams buried. To prevent clams from 4 cm of the tubes was filled with sediment. Clams escaping the January 1988 burial cages, an addiwere placed on top of this sediment base and the tional piece of 1 mm mesh screen was placed on rest of the tubes were filled with sediment. Be- top of the clams before packing the rest of the tween 40 and 50 clams of varying sizes were tube with sediment. This was the only difference in the experimental design between the spring and placed in each tube. A hole approximately 0.5 m2 and 0.4 m deep winter burials. The original design called for retrieving two was excavated at the Om (MLLW) tidal level. The burial tubes were placed in the hole about tubes each at two-week, two-month, and eight2 cm apart and the tops of the tubes were about month intervals, from both the spring 1987 and 20 cm below the sediment water interface (thus winter 1988 burials. The landmark we used to
356 Michael P. Russell arid others
LETHAIA 25 (1992)
Fig. 2. Cross-polarized light micrographs of Trunsemiella confusu broods from three different phases of the reproductive cycle: i7 A Spring: L1 6 . Summer and Fall; 0 C. Winter. The calcified embryonic valves refract light and are brightly illuminated. In each micrograph the earliest stages of development (including the uncalcified embryos) are between 230 and 250 pm. and the later stages of development (including the fully formed juveniles) have valve lengths between 550 and 580 Fm.
relocate the exact burial site was removed by the San Mateo County Park and Recreation Department before we could retrieve the last two burial cages. Despite many excavations, the last two cages were lost and we only have data for the winter samples from the two-week and twomonth burials.
Results and discussion The earliest stages of embryos observed in a brood are between 230 and 250 pm and the largest are between 550 and 580 pm (Fig. 2). There is seasonal variation in both aspects of brood structure, i.e.. total number of embryos and relative frequencies of the, different size classes (Russell & Huelsenbeck 1989). Spring and winter exhibit the most disparate brood structures. Fecundity levels are lowest in winter, but the broods are dominated by the larger size classes, whereas spring fecundity levels are high and the broods are dominated by the smallest size class. Fig. 2 shows cross polarized light micrographs of typical brood masses from three different phases of the reproductive cycle. Although fecundity levels are higher in the spring, the fossilization potential of these broods is low because most of the embryos are in the earliest stages of developmental and lack calcified valves.
The winter broods show the greatest potential for fossilization despite having the lowest fecundity levels because the majority of the embryos are in the later stages of development and have calcified valves (Fig. 2). Because number of embryos is a function of adult size (Kabat 1985; Russell & Huelsenbeck 1989), we restrict the presentation of the burial data to adults between 3 and 5 mm. The development of calcified valves occurs between 250 and 300 pm. As expected, all uncalcified embryos are lost during the first two weeks in both the spring and winter burials (Fig. 3). The greatest taphonomic impact occurs during the spring because these clams contain broods which are dominated by the smallest size class of embyros and lack calcified valves (Fig. 2). The presence of all four size classes of embryonic valves in clams from both the spring and winter burials suggests that the asynchronous mode of brooding is potentially preservable in the fossil record (Fig. 3). Although these results are only from burials of two and eight weeks, the partial results from the eight-month spring burial experiment support this conclusion. There were nine brood bearing adults recovered from the eight-month spring burial cages and embryonic valves from all but the smallest size class were found inside articulated adults. Fig. 4 contrasts the original size distribution of the spring broods
357
Ezcperimentul tuphonomy of brooding bivalve
LETHAIA 25 (1992)
Winter
40
P Fig. 3. Average number of embryos in four different size classes of development from adults 3 to 5 mm long. The 0 week burial data are dissections of live clams indicating the original levels of fecundity and brood structure for the spring ( I S May 1987) and winter (19 January 1988) seasons. Points are k 1 standard deviation.
2000
0
2
0
2
8
Weeks Since Burial
with the sizes of embryos found after the eightmonth burial treatment. Some of the adults clams from the burial experiments were found gaping and contained sediments mixed in with the remains of the embryonic valves. These clams generally contained fewer embryonic valves than those that were closed tightly and did not contain sediments. The presence of sediment inside articulated clams indicates the movement of particles between the surrounding matrix and the mantle cavity of the clams. The valves of the smaller developing embryos are the same size as some of the sediment particles. Therefore, it is reasonable to infer that at least some of the smaller embryonic valves were lost to the surrounding matrix. Transennellu specimens were collected from the Etchegoin formation of the Kettleman Hills on 3 August 1986 (Fig. 1, UCMP D-9929). A total of 20 articulated individuals were recovered and 5 of these contained sediment. Of the 15 that were not sediment-filled, 3 contained traces of embryonic valves. One of the clams contained
A N=23 Adults
loo0
"500
Embryo Sizes (pm)
Fig. 4. Size distributions of the embryonic valves. 0 A. Total distribution of spring pre-burial embryonic valves. 0 B. Size distribution of embryonic valves recovered from the 8-month spring burial cages. A total 209 pairs of embryonic valves were recovered from nine adults. All but the earliest stages of development were recovered.
358 Michael P. Riissell and others
LETHAIA 25 (1992)
FIR. 5. Scanning electron micrograph of a Transennelh sp. brood recovered from the Kettleman Hills Etchegoin Formation of California (UCMP 37442). Various stages of embryonic valve development are apparent in this specimen, indicating the asynchronous mode of development (scale bar 550 pm)
a well-preserved asynchronous brood (Fig. 5). It is clear that the size classes of developmental stages represented in this specimen are comparable to the range of size classes present in Trunsennellu confusu today (compare Fig. 5 with Fig. 2). This establishes the asynchronous brooding mode of reproduction in Trunsennellu in the Late Miocene to Early Pliocene; the Etchegoin formation was dated by Obradovich et al. (1978) to 7.0 2 1.2 Myr BP with the Fission-Track method on zircon. This fossil also supports the results of the burial experiments showing the preservation of the different stages of embryonic valve development. Although it is possible that both the synchronous and asynchronous modes of brooding reproduction were present in Transennella in the Etchegoin formation and only the asynchronous mode survived to the Recent, this evolutionary scenario seems unlikely. Several of the clams from the winter burial experiments contained only the large size classes of embryos. These
apparent synchronous broods probably resulted from the loss of the earlier stages of the development due to gaping. The fossil synchronous broods may represent a similar situation, i.e., the lack of preservation of the earlier stages of development during a specific phase of the reproductive cycle. The results of the burial experiments and UCMP 39828 (Fig. 5 ) indicate that asynchronous brooding in Transennella has been a conservative life history trait since at least the Pliocene. A cladistic treatment of the evolution of life history strategies in small venerid bivalves also supports this interpretation (Lindberg 1990). Acknowkdgmmls. - The Museum of Paleontology a t the University of California provided financial support in the form of the Alexander Fellowship and Palmer Award to MPR. Carole Hickman, James Valentine, Wayne Sousa, and Peter Rodda commented on earlier drafts of the manuscript. We also thank Diarmaid OFoighil and an anonymous reviewer for their constructive criticisms. Charlotte Fiorito assisted with photography and Michael LaBarbara showed us the cross-polarized lighting technique.
LETHAIA 25 ( 1992)
References Armstrong, L. R. 1965: Burrowing limitations in Pelecypoda. The Veliger 7, 195-200. Chaffee, C. & Lindberg, D. R. 1986: Larval biology of early Cambrian molluscs: the implications of small body size. Blrlletin sf Marine Science 39, 536-549. Chaffee. C . & Strathmann. R. R. 1984: Constraints on egg masses. I. Retarded development within thick egg masses. Journul of Esperimental Marine Biology und Ecology 84, 73-83. Gallucci, V. F. & Kawaratani. R. K. 1975: Mortality of Transennella tanlillu due to burial. Journal of the Fisheries Reseurcli Board of C a n a h 32, 1637- 1640. Giese, A. C., Pearse, J. S. & Pearse, V. B. (eds.) 1987: Reproduction of Mnrine Invertebrutes. Vol. IX. 712 pp. Blackwell Scientific Publications, Palo Alto. Gray, S. 1982: Morphology and taxonomy of two species of the genus Trunsennellu (Bivalvia: Veneridae) from western North America and a description of T. confusa sp. nov. Malucolngiral Review 15, 107-117. Kabat, A. R. 1985: The allometry of brooding in Transennella taritilla (Gould) (Mollusca: Bivalvia). Journal of Esperimental Murine B i o l o ~ yond Ecology 9l. 271 -279 Lindberg, D. R. 1984: Fossil brooding bivalve molluscs from the Neogene of western North America. Geological Society of America. Abstracts with Programs 16, 576.
Experimental taphonomy of brooding bioah~e 359 Lindberg, D. R. I990 Transennella Dall versus Nutricolu Bernard (Bivalvia Veneridae): an argument for evolutionary systematics. Journul n/' Molluscan Studies 56, 129- I52 Obradovich, J. D., Naeser, C. W. & Izett. G. A. 1978: Geochronology of Late Neogene marine strata in California. Stanf o r d Uniiw-sity Publications in Geological Sciences 14, 40-41. Rosenberg, G. D. 1980:An ontogenetic approach to the environmental significance of bivalve shell chemistry. I n Rhoads. D. C. & Lutz, R. A. (eds.): Skeletal Growth
