Proc. Natl. Acad. Sci. USA Vol. 83, pp. 6912-6914, September 1986 Evolution Mass extinctions: Sensitivity of marine larval types (Permian-Triassic, Cretaceous-Tertiary extinctions/bolide impact/developmental strategy) JAMES W. VALENTINE* AND DAVID JABLONSKIt *Department of Geological Sciences, University of California, Santa Barbara, CA 93106; and tDepartment of the Geophysical Sciences, University of Chicago, Chicago, IL 60637 Contributed by James W. Valentine, June 6, 1986 ABSTRACT Developmental types of marine invertebrates mechanism is occlusion of the sun by dust and smoke clouds, may be divided into planktotrophs, which feed on suspended successively lowering temperatures, suppressing primary food items, and nonplanktotrophs, which do not feed but are productivity, and severing food chains in an extreme pertur- supplied with nutrients (yolk) parentally; these may represent bation estimated to have lasted from 6 months to 2 years (14). high mortality-fecundity and low mortality-fecundity strate- Evidence for a bolide impact near the K-T boundary is strong gies, respectively. Most versions ofthe bolide impact hypothesis (12, 15-19), though not conclusive (20). There are also of mass extinction propose occlusion of the sun by dust or reports, not yet confirmed by outside laboratories, of similar smoke and severance of planktonic food chains for months or evidence at the P-Tr boundary in China (21, 22), although a few years, and this should select preferentially against whether this relates to a local or a more general event is not planktotrophs. Yet among fossil prosobranch gastropods, yet clear. planktotrophs survived the end-Cretaceous extinction equally Many scenarios for mass extinction by bolide impact at the as well as nonplanktotrophs. Indirect evidence suggests that K-T boundary rely on the plankton crisis to drive the end-Permian extinctions may have selected against plankto- extinction of marine benthic invertebrates via their plank- trophs but that the effect was prolonged over millions of years. tonic larval stage in the life cycle (23-25). This extinction mechanism can be examined directly for marine gastropods Comparative studies of the effects of marine invertebrate based on scanning electron microscopy of fossil larval shells adaptive strategies on evolutionary rates and patterns have (1-6, 8). For those gastropod lineages for which unequivocal led to explanatory models for the differential survival of larval data are available, the two larval types do not exhibit clades with contrasting larval types (1-7). Applied to mass significant differences in survivorship: of the 51 North extinctions at the Cretaceous-Tertiary (K-T) and Permian- American Coastal Plain genera for which larval types have Triassic (P-Tr) boundaries, the larval data put significant been inferred from larval shell morphologies, 11 of 28 constraints upon the mechanisms that could have been planktotrophs (39%) and 9 of 23 nonplanktotrophs (39%) responsible-constraints that are at variance with most survived the end-Cretaceous extinction (Table 1). This ap- current models for mass extinctions triggered by extrater- pears to rule out a brief, catastrophic plankton crisis as the restrial impacts. primary extinction mechanism. A simple dichotomy of planktotrophic and nonplankto- It might be argued that the predicted plankton crisis would trophic larval types is sufficient for our purposes; it has be so brief that it would have little effect on differential operational utility in much of the fossil record and represents survivorship but would simply impose a year's recruitment important modalities in invertebrate life histories (8). Species failure on planktotrophs. Adults might wait out the crisis and with planktotrophic development rely on the plankton for then return to reproduction as usual. However, the K-T larval nutrition and have small yolk-free eggs, which can be extinction involved the extirpation of about 50% of marine produced in great numbers; species with nonplanktotrophic genera (26) and perhaps 75% of marine species (27). If this development must supply food to embryos and/or larvae, occurred as a single brief catastrophic event, it implies that usually as yolk, and thus generally produce far fewer eggs per enormous numbers of adults were killed, perhaps in the 90% female. Interpretation of the adaptive significance of the range, and that many, perhaps most, of the marine popula- pattern of these larval modes among the living marine fauna tions that survived did so by a narrow margin. For those is controversial, but a common suggestion is that these endangered species, the lack of a year's recruitment could strategies represent a trade-off between mortality and fecun- easily prove decisive. Furthermore, rebound to a healthy dity (9). It is clear that lineages with either strategy persist in productive oceanic ecosystem would not have occurred in a most environments for millions of years; presumably a single year, so that the stress associated with the plankton lineage may be highly fecund but endure high larval mortality crisis should have extended for a number of years, and such or may have low fecundity but enjoy lower larval loss. stress would be more significant for planktotrophs. It is Nevertheless, planktotrophic larvae must rely upon the difficult to see how a plankton crisis of such proportions as planktonic food web and are dominant in warm, shallow, to lead to a mass extinction would not favor nonplankto- low-latitude waters wherein trophic supplies for larvae are trophs. relatively steady (10, 11). Another test of the effects of a plankton crisis is in the We have investigated the marine mass extinction events at patterns of extinctions among inferred planktotrophs of the K-T and P-Tr boundaries with regard to their effects on differing generation time. At present, generation times can be larval types. In recent years, bolide impacts have been inferred only indirectly, but lifespan and generation time in proposed as forcing mechanisms for some or all of the major mollusks are roughly correlated with body size: annuals and mass extinctions in the fossil record (12, 13). For the K-T other short-lived species tend to be small, and large-sized boundary, it has been suggested that the proximal extinction species tend to be long-lived (e.g., refs. 28 and 29). Therefore, the prediction would be that large-bodied mollusks should The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" Abbreviation: K-T and P-Tr boundaries, Cretaceous-Tertiary and in accordance with 18 U.S.C. §1734 solely to indicate this fact. Permian-Triassic boundaries. 6912 Downloaded by guest on September 30, 2021 Evolution: Valentine and Jablonski Proc. Natl. Acad. Sci. USA 83 (1986) 6913 Table 1. Survivorship among planktotrophic and nonplanktotrophic Table 2. Orders of durably skeletonized marine invertebrates gastropod genera of the Gulf and Atlantic Coastal Plain during the that first appeared during the Triassic end-Cretaceous mass extinctions Living relatives (R) Victims Survivors or members (M) Planktotrophs 17 11 Order Status planktotrophic? Nonplanktotrophs 14 9 Early Triassic Survivorship was 39% in both groups. Spongiomorphida Extinct No (R) Unionida Living No (M)* more successfully weather the hypothesized brief plankton Phyllocerida Extinct No (R) crisis than should small-bodied mollusks. However, large- Medial Triassic bodied planktotrophic molluscan genera, inferred to have Hexactinosida Living No (M) been long-lived (e.g., bivalves Exogyra, Arctostrea, Veni- Scleractinia Living Yes (M)t ella, Pachycardia, and Costellacesta and gastropods Trobus, Millericrinida Living No (M) Drilluta, and Longoconcha), suffered marked extinction at Isocrinida Living No (M) the K-T boundary. Survivorship of bivalve and gastropod Roveacrinida Extinct No (R) genera, whose species exhibit a median body size (estimated Late Triassic by using geometric mean of height and length) of >4 cm, is ?Lychniscosidae Living No (M) 31% (n = 36), whereas survivorship among genera of <4 cm Diadematoida Living Yes (M) is 41% (n = 160) (0.01 < P < 0.05, binomial proportions test) Pedinoida Living Yes (M) (D.J., unpublished data). Furthermore, a number of small- Hemicidaroida Extinct Yes (R) bodied planktotrophic genera, likely to have been annuals or Plesiocidaroida Extinct Yes (R) short-lived on the basis of their living relatives, survived the *Living members are nonmarine. mass extinction (e.g., Cerithium, Seila, Eulima, and tPlanktotrophic members are rare. Aciculiscala). Survivorship among the small (<1 cm) bivalves and gastropods believed to be planktotrophic was The patterns of larval extinction associated with the K-T 44% (n = 50), not significantly different from survivorship in and P-Tr extinctions do not conform to most bolide impact larger planktotrophs (D.J., unpublished data). The conclu- scenarios. The K-T extinction factors cannot have complete- sion is that long-lived planktotrophs did not enjoy an advan- ly severed the planktonic marine food chains or greatly tage (nor were short-lived or annual planktotrophs at a destabilized the productivity regimes, or planktotrophs disadvantage) at the K-T boundary, again falsifying the would have been preferentially extinguished. Among predictions for the killing mechanism as a brief plankton planktotrophs, taxa with short generation times should have crisis. suffered most heavily, and long-lived taxa should have been The P-Tr