Research ArticleOCEANOGRAPHY

Algal plankton turn to hunting to survive and recover from end-Cretaceous impact darkness

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Science Advances  30 Oct 2020:
Vol. 6, no. 44, eabc9123
DOI: 10.1126/sciadv.abc9123
  • Fig. 1 Stratigraphic distribution and trophic strategy of selected survivor and incoming nannoplankton taxa.

    Important survivor taxa are indicated on the left, and incoming species are indicated on the right with an indication of principal trophic mode [based on our assessments, (24), Table 1, and table S1]: mixotrophs in blue and autotrophs in green. Bar thickness is a qualitative indication of abundance, with the broadest bars showing acme abundances. Dashed lines indicate dominantly coastal or neritic distributions. Close phylogenetic relationships are shown by arrows. The ancestry of Cruciplacolithus is uncertain but may lie with the Biscutaceae. The nannoplankton data are primarily from our work but are largely consistent with published sources. NP, nannofossil biozone.

  • Fig. 2 Modern and fossil coccolithophore cell wall coverings.

    (A and B) Scanning electron microscopy (SEM) image showing disarticulated coccoliths (A) and complete coccosphere (B) [Danian, Newfoundland Ridge, Integrated Ocean Drilling Program (IODP) Site 1407 sample 1407A-23-2, 50 cm]. (C) Light microscope (LM) image showing modern coccospheres of Coccolithus in culture as an example of nonflagellate, diploid, heterococcolith coccospheres. Cells from culture experiments performed in (58) using a North Atlantic open ocean isolate RCC1197. (D) SEM and LM images of complete Danian diploid, heterococcolith coccospheres with flagellar openings (additional examples in fig. S2). The SEM Praeprinsius are from Newfoundland Ridge (upper specimen from sample 1407C-20-4, 125 cm, and lower from sample 1407A-23-2, 35 cm). Prinsius from a North Sea well sample (see table S2) and both Futyania are from Blake Nose sample 1049C-8-4, 38 cm. The LM images of Praeprinsius are from 1407A-23-2, 50 cm, and those of Futyania are from 1407C-20-4, 125 cm. Modified circumflagellar coccoliths are shown in green for Futyania. (E) Modern coccospheres with flagellar openings [from (27)]. (F) LM image showing cell (Prymnesium parvum) with flagella (f) and haptonema (h) [from (26)].

  • Fig. 3 Fossil nannoplankton abundance of flagellate cells and species richness.

    On the left is the percent flagellate cells (24) from sites in the South Atlantic (ODP Site 1262, dark blue), North Atlantic (IODP Sites 1403 and 1407, brown), and the palaeosubequatorial Pacific (ODP Sites 1209 and 1210 and DSDP Site 577, light blue). The percent flagellate cell abundances for the Upper Cretaceous (dashed blue lines) are shown as the percentage of coccolithophores of unknown ecology, of which there may be some flagellate taxa (24), providing us with a maximum possible estimate. The position of the red star indicates our suggestion that all taxa that survived across the K/Pg boundary were capable of phagotrophy. Paired-sample t tests, comparing the percentage of flagellate cells between the early Danian (up to 64.2 Ma) and both the Late Cretaceous and the later Danian (after 64.2 Ma), indicate significant differences between communities in all cases (see table S3). On the right is the high-resolution (number of species present per 100 ka) fossil calcareous nannoplankton species richness (10). Milestones in ecosystem recovery in the post-extinction ocean are indicated (10, 11). Paleogene data are shown against age. The Cretaceous data are a representative uppermost portion, with no high-resolution age assignment (24).

  • Fig. 4 Evolution of traits in the model plankton community.

    The tree structure describes the evolutionary development of the community, with the trajectory of each branch describing changes in the trophic strategy and size of an individual population through time. With time progressing from the bottom up, evolutionary changes to traits are represented by changes in the horizontal position (and color) of its respective branch in the tree. Speciation occurs when one branch divides into two. The inset panel shows a more detailed view of the tree for the region bounded by the gray box, broadly corresponding with the cell size range of coccolithophores. The shape of the tree is technically defined by a three-dimensional surface contour (trophic strategy, size, and time) inside which population biomass exceeds 0.01 mmol N−1 m−3. Note that mutation and evolution proceed much faster in the model because the model applies a simplified trait diffusion approach to evolution (24).

  • Fig. 5 Evolution of the plankton community and the fitness landscape through time.

    Each panel represents two-dimensional “trait space” of trophic strategy and equivalent spherical diameter (ESD; in micrometers). Background colors (red to blue) describe changes in fitness landscape through time, with height equivalent to biomass-specific net population growth rate. Dots indicate extant populations, with area proportional to population size and color (green to magenta) indicating the balance of autotrophic and heterotrophic nutrition. At year 1, biomass is low and inorganic resources are high, and we see a peak in the fitness landscape centered on fast growing autotrophic cells. By year 2, the population has increased, and a new peak in the fitness landscape has emerged for larger and more heterotrophic traits driven by this potential prey. Over the next 100 years or so, the initial population adapts toward the new fitness landscape peak, with small mixotrophs coexisting with the initial photoautotrophic population. After approximately 100 years, the community has gained sufficient size diversity to begin showing predator-prey dynamics. The evolving community then branches, heading toward the stable coexistence of small phytoplankton, intermediate mixotrophs, and larger zooplankton. At year 5000, it can be seen that there are no remaining positive regions of the fitness landscape, indicative of a community at an ecological and evolutionary equilibrium.

  • Table 1 Description, images, and ecology of nannoplankton taxa that are found as fossils in the Upper Cretaceous and survive the K/Pg mass extinction event.

    Coccosphere morphology is based on observation of preserved coccospheres except for Calciosolenia, which is based on the shape of the coccosphere in its living species. Neocrepidolithus, Zeugrhabdotus, Lapideacassis, and Octolithus are extinct taxa that have never been observed as intact coccospheres, but modern coccospheres of taxa with the same coccolith morphology (muroliths) as Neocrepidolithus and Zeugrhabdotus tend to have very high lith numbers and are typically found in more coastal areas. Information about living relatives can be found summarized in (27). Survival mechanism listed here is based on whether we consider that their ecology and/or coccosphere morphology points to potential mixotrophy. Markalius is the most ambiguous as they form typical placolith-morphology coccospheres that are spherical and have low Cn (number of coccoliths per coccosphere) and no openings. Source of SEM images: (27, 38, 73). The coccosphere next to Octolithus is a representative modern holococcolith coccosphere (27). SEM images are not to the same scale.

    Survivor taxon and familyCoccosphere
    living relative ecology
    Survival mechanism(s)Rationale
    Embedded ImageImperforate dodecahedron
    in calcified phase (seen as
    Coastal, coastalMixotrophy in dominant,
    noncalcified motile phase,
    possible resting cyst (the
    dodecahedron coccosphere),
    *Coastal distribution, mixotrophy,
    and dominance of motile phase
    have been documented (68, 69),
    and calcified resting cyst stage is
    highly likely (Hagino pers. comm.).
    In addition, extant forms have
    endosymbiotic cyanobacteria (70).
    Embedded ImageImperforate sphereCoastal, coastalCoastal mixotrophy, existed
    in dominant motile
    (noncalcified) phase?
    †Coccolith-bearing phase shows
    no evidence for a flagellar
    opening, but modern dominant
    phase (noncalcified) is likely
    motile, and coastal ecology points
    to mixotrophy (68).
    Embedded ImageEllipsoidal to cylindrical
    with possible flagellar
    Coastal, coastalCoastal mixotrophy.Ellipsoidal coccosphere with
    potential flagellar openings plus
    coastal/near-shore ecology (19, 71)
    points to mixotrophic capacity.
    Incertae sedis
    Embedded ImageImperforate sphereCoastal, extinctCoastal mixotrophy?No evidence for a flagellar
    opening but coastal ecology
    could point to mixotrophic
    capacity. Similar to
    Embedded ImageUnknown, similar to
    modern murolith spheres
    with high Cn?
    Coastal, extinctMixotrophy?Coastal ecology and potentially
    high Cn could point to
    mixotrophic capacity. Many
    modern coastal murolith species
    are flagellate [see (27)].
    Embedded ImageUnknown, similar to
    modern murolith spheres
    with high Cn?
    Coastal, extinctMixotrophy?High latitude and coastal ecology
    (19), plus potentially high Cn could
    point to mixotrophic capacity.
    Many modern coastal murolith
    species are flagellate [see (27)].
    Embedded ImageUnknownCoastal, extinctMixotrophy?Unusual coccolith morphology
    and atypically restricted coastal
    ecology point to mixotrophic
    Embedded ImageFusiform with flagellar
    Coastal, coastalMixotrophyStrongly fusiform coccosphere
    with flagellar openings plus
    coastal ecology (72) points to
    mixotrophic capacity.
    Embedded ImageImperforate dodecahedronCoastal, extinctResting cyst and/or
    Similar morphology to
    Braarudosphaera could suggest
    similar ecology, but atypical
    restricted coastal ecology also
    points to mixotrophic capacity.
    Embedded ImageHolococcolith, unknown
    Coastal, extinctMixotrophyLiving holococcolith-phase
    coccolithophores are typically
    flagellate‡, and coastal ecology
    also points to mixotrophic

    *Modern Braarudosphaera is highly anomalous among coccolithophores in having a possible resting phase and endosymbionts.

    Cyclagelosphaera, while exhibiting a typical imperforate coccosphere in its calcifying phase, again appears highly anomalous as modern observations indicate that it is coastal and only exists for a short time in this life-cycle phase (68).

    ‡Holococcoliths are specific to the haploid phase of coccolithophores that is characteristically motile (25).

    Supplementary Materials

    • Supplementary Materials

      Algal plankton turn to hunting to survive and recover from end-Cretaceous impact darkness

      Samantha J. Gibbs, Paul R. Bown, Ben A. Ward, Sarah A. Alvarez, Hojung Kim, Odysseas A. Archontikis, Boris Sauterey, Alex J. Poulton, Jamie Wilson, Andy Ridgwell

      Download Supplement

      The PDF file includes:

      • A Matrix Community Model
      • Figs. S1 to S7
      • Tables S1 to S4
      • References

      Other Supplementary Material for this manuscript includes the following:

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