1. What the deep sea tells us about sampling biases
in the fossil record
Graeme T. Lloyd
Department of Palaeontology, Natural History Museum, London, UK

2. Collaborators
Andrew Jeremy Paul
Smith Young Pearson

3. Talk Outline
• Introduction
• Deep sea record of Coccolithophores and planktic forams
– Deep sea rock and fossil records
– Correlations and modelling
– Sampling-corrected richness
• Deep sea vs. land-based record of Coccolithophores
– Deep sea vs. land rock and fossil records
– Correlations and modelling
– Sampling-corrected richness: common signal?
• Deep sea coccolithophore species-per-genus patterns
– An unusual result!
– Potential explanation(s)
– Separating signals
• Conclusion

4. The fossil record is our only empirical record of the
history of life

5. Land-based rock and fossil records show strong
correlation…
N Maps
Generic diversity

6. …but what about the deep sea?
•Most microfossil groups are highly cosmopolitan…
•…and massively abundant (1000s specimens per gram)
•Many remarkably continuous sections (>10 million years)
•Phylogenies often incorporate ancestors
•Well studied (DSDP/ODP/IODP)
•The best fossil record we have?

7. Comparing coccolithophore and planktic foraminifera
deep sea rock and fossil records
•Questions:
•How does the deep sea rock record change over time?
•How does the deep sea fossil record change over time?
•Are the deep sea rock and fossil records correlated?
•How do the two major calcareous groups compare?

8. The database
Coccoliths Planktic forams
•35,416 species occurrences •19,349 species occurrences
•16,197 samples •3,850 samples
•205 sites •135 sites
•4,329 names •2,462 names
Geotectonic history

9. Rock record
Coccoliths Planktic forams

10. Species record
Coccoliths Planktic forams

11. Generic record
Coccoliths Planktic forams

12. Species correlation
Coccoliths Planktic forams

13. Generic correlation
Coccoliths Planktic forams

14. Species detrended
Coccoliths Planktic forams

15. Genera detrended
Coccoliths Planktic forams

16. Subsampling
Coccoliths Planktic forams

17. Modelled versus observed diversity
Coccoliths Planktic forams

18. Model-corrected diversity
Coccoliths Planktic forams

19. Summary
•How does the deep sea rock record change over time?
•Exponential rise (opening ocean basin)

20. Summary
•How does the deep sea rock record change over time?
•Exponential rise (opening ocean basin)
•How does the deep sea fossil record change over time?
•Coccolith species ~linear rise
•Coccolith genera ~rapid rise followed by slow fall
•Forams: double sawtooth (K-T divides)

21. Summary
•How does the deep sea rock record change over time?
•Exponential rise (opening ocean basin)
•How does the deep sea fossil record change over time?
•Coccolith species ~linear rise
•Coccolith genera ~rapid rise followed by slow fall
•Forams: double sawtooth (K-T divides)
•Are the deep sea rock and fossil records correlated?
•Yes, strongly

22. Summary
•How does the deep sea rock record change over time?
•Exponential rise (opening ocean basin)
•How does the deep sea fossil record change over time?
•Coccolith species ~linear rise
•Coccolith genera ~rapid rise followed by slow fall
•Forams: double sawtooth (K-T divides)
•Are the deep sea rock and fossil records correlated?
•Yes, strongly
•How do the two major calcareous groups compare?
•Forams seem to be less biased than coccos

23. Comparing sampling bias between the land and the
deep sea

24. Testing sampling bias versus common cause
Deep sea Land
•Correlations between sampling and diversity are common
•Two main explanations: sampling-bias and common cause
•For coccolithophores we have two records; ideal to test
•Sampling-bias predicts diversity will track sampling
•Common cause predicts shared diversity
•What do the two rock records look like?
•What do the two fossil records look like?
•Are the rock and fossil records correlated?
•Is there evidence for a common palaeobiodiversity?

25. The database
Deep sea Land
205 sites, 16,197 samples, 462 sections, 5,563+ samples,
36,416 occurrence records 22,745 occurrence records

26. Rock records
Deep sea Land
Number of cores recovering Number of localities with
rock of given age published nannofossil
taxonomic lists
Time (Ma) Time (Ma)

27. Species richness
Deep sea Land
Raw species diversity
Number of species Number of species
Time (Ma) Time (Ma)

28. Species richness versus rock record (1): raw data
Deep sea Land
Log (Nsites) Log (Nsites)
Log (species richness) Log (species richness)

29. Species richness versus rock record (2): first differences
Deep sea Land
Log (Nsites) Log (Nsites)
Log (species richness) Log (species richness)

30. Estimating true diversity: 1, subsampling
Deep sea Land
109 samples per bin 106 samples per bin
Species diversity (max) Species diversity (max)
Time (Ma) Time (Ma)
Orange = empirical pattern
White = diversity at equal subsampling

31. Estimating true diversity: 2, modelling
Deep sea Land
True richness modelled as invariant (observed richness = sampling)
Species richness Species richness
Time (Ma) Time (Ma)
Yellow = empirical pattern
Blue-green = model prediction assuming diversity is
invariant and shaped by rock abundance

32. Estimating true diversity: 2, modelling
Deep sea Land
Residuals from modelled richness
Time (Ma) Time (Ma)

33. Estimating true diversity: 3, alpha diversity
Deep sea Land
Mean number of species recorded per site
Species Species
Time (Ma)
Time (Ma) Time (Ma)

34. Summary
Deep sea Land
• The recorded history of coccolithophorid diversity over
last 150 Ma changes dramatically according to whether
data is drawn from land-based records or deep-sea
records
• Coccolithophorid diversity correlates strongly to the shape
of the rock record it is recovered from
• Subsampling, modeling and estimates of mean alpha
diversity all point to a third, much more uniform diversity
irrespective of which record is used

35. Species per genus patterns

36. Higher taxa as species proxies
• Used since the earliest diversity curves…
• …and continue to be (e.g. Alroy et al. 2008)
• Originally pragmatic (less data required)
• Then argued that species are inadequate
• But, adequacy of higher taxa to represent species-level
patterns is essentially untested

37. Taxonomic level affects pattern

38. Flessa and Jablonski 1985
• Only explicit test of
species-to-higher taxon
ratio
• Compared families to
number of named
species in Zoo. Record
(Raup 1976)
• Pattern of change
differs
• Families become more
speciose

39. Our database is superior
• Species are standardised (synonyms)
• Species are assigned to genera
• Species are often widespread
• Species are long-ranging
• Species are comparatively stable taxonomically
• Questions:
• How does the species-to-genus ratio change over time?
• How does the sampling change over time?
• How does the number of taxonomists change over time?
• Do neither, either or both sampling and taxonomists shape
the signal?

40. Species per genus

41. Number of sites (sampling)

42. Number of authors (taxonomists)

43. Long-term correlation (raw)
N sites (rho = 0.95)
N authors (rho = 0.93)

44. Short-term correlation (sampling)
Species per genus Rho = 0.43
N sites

45. Short-term correlation (taxonomists)
Species per genus Rho = 0.44
N authors

46. Correlations
• Both number of sites and number of authors significantly
correlate with species-per-genus
• Fit 3 models:
– spg ~ N sites
– spg ~ N taxonomists
– spg ~ N sites + N taxonomists
• Which is the best explanatory model?
– Akaike weights = N Sites (marginally more than a
combined model)
– Variance partitioning = a combined model
• So is it sites or combined?

47. Subsampling (rarefaction by occurrences for sites)

48. Subsampling (rarefaction by occurrences for papers)

49. Summary
• How does the species-to-genus ratio change over time?
– In a two-step ‘punk eek’ way

50. Summary
• How does the species-to-genus ratio change over time?
– In a two-step ‘punk eek’ way
• How does the sampling change over time?
– The same

51. Summary
• How does the species-to-genus ratio change over time?
– In a two-step ‘punk eek’ way
• How does the sampling change over time?
– The same
• How does the number of taxonomists change over time?
– The same

52. Summary
• How does the species-to-genus ratio change over time?
– In a two-step ‘punk eek’ way
• How does the sampling change over time?
– The same
• How does the number of taxonomists change over time?
– The same
• Do neither, either or both sampling and taxonomists shape
the signal?
– Both contribute to the pattern

53. Summary
• How does the species-to-genus ratio change over time?
– In a two-step ‘punk eek’ way
• How does the sampling change over time?
– The same
• How does the number of taxonomists change over time?
– The same
• Do neither, either or both sampling and taxonomists shape
the signal?
– Both contribute to the pattern
Genera are not an accurate proxy for species

54. Conclusion: what does the deep sea tells us about sampling
biases in the fossil record?
• The deep sea record shows the same correlation with
sampling as land-based studies
• This argues in favour of the sampling-bias interpretation
and not the common cause
• The deep sea record is more biased than the land-based
• The deep sea coccolithophore record is more biased than
the deep sea planktic foram record
• Once sampling has been accounted for there is
convergence on a single palaeobiodiversity estimate (at
least for Coccolithophores)
• Taxonomic structure (species-per-genus) for deep sea
Coccolithophores is biased by both sampling and the
number of taxonomists