Deep-Sea Research II 47 (2000) 1679}1700

Calculation of coccolith volume and its use in

calibration of carbonate flux estimates
Jeremy R. Young *, Patrizia Ziveri

Palaeontology Department, The Natural History Museum, London, SW7 5BD, UK

Vrije Universiteit Amsterdam, Faculteit der Aardwetenschapen, Amsterdam, NL, The Netherlands
Received 13 February 1998; received in revised form 22 December 1998; accepted 5 January 1999

Abstract

Estimates of coccolith volume help in determining total coccolith carbonate #uxes and the
relative contributions of various coccolith species. It is argued here that the best approach to
deriving such coccolith volumes is to calculate shape factors, k , for each species separately

based on reconstruction of cross pro"les and to determine mean sizes from measurement of size
variation in the sample of interest. Then volume"k l. Values of k are given for the most
 
important extant coccolith species based on reconstruction of cross-sections, followed by
calculation of a volume of rotation using an iterative routine implemented in an image analysis
package. Substantial errors, ca. 50%, are inevitable in such calculations, but the resultant data
are nonetheless of value. Coccolith assemblages from North Atlantic (473N 203W) JGOFS 1989
sediment trap samples are analysed as a test case; calculated coccolith PIC #uxes constitute
30}80% of the chemically determined total PIC #uxes.  2000 Elsevier Science Ltd. All rights
reserved.

1. Introduction

Calculation of #uxes of matter within the oceanic water column has become
a major research endeavour over the last decade (e.g., Beaufort and Heussner, 1999;
Broerse et al., 2000; Ziveri et al., 2000). This re#ects the importance of oceanic #uxes
within global biogeochemical cycles, most notably the carbon cycle. In addition, it
re#ects the development of sediment traps that allow sampling of particulate #uxes
over "nite time periods. Total #uxes of matter are best determined by chemical or

* Corresponding author. Tel.: 44-171-938-8996; fax: 44-171-938-9277.

E-mail addresses: jy@nhm.ac.uk (J.R. Young), zivp@geo.vu.nl (P. Ziveri).

0967-0645/00/$ - see front matter  2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 9 6 7 - 0 6 4 5 ( 0 0 ) 0 0 0 0 3 - 5
1680 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700

physical measurement, but to probe the biotic component of the biogeochemical

system in any depth we require breakdown of #uxes at least by organismal group. For
this, an attractive methodology is to convert specimen accumulation rates into mass
#uxes. The methodology is attractive since biologists and micropalaeontologists
routinely conduct per taxon specimen counts to investigate other questions. For
instance, study of coccoliths in sediment trap samples may be carried out in order to
study ecological succession, sedimentation processes or biogeography, but in all cases
routine analysis includes counts of the abundance of coccoliths, identi"ed to species
level. Converting these count data into per species carbonate #ux estimates is a trivial
problem, if accurate estimates of coccolith volume can be obtained.
In the case of coccoliths, we are particularly interested to quantify mass #uxes since
they are widely believed to be a major, if not dominant, contributor to open-oceanic
carbonate #uxes. Moreover, since it is di$cult to separate coccoliths from other
sediment particles, conversion of taxon counts seems an obvious approach for
calculation of #ux rates. The methodology is also potentially applicable to
palaeoceanographic studies * methods for calculating accumulation rates of cocco-
liths in sediment cores (i.e., specimens deposited per unit area per unit time) are
becoming increasingly reliable and widely used (e.g., Su, 1996; Flores et al., 1997).
Given reliable estimates of coccolith mass, this data can easily be converted into
species-speci"c mass #uxes.
Several estimates of coccolith volume have been published (Paasche, 1962; Honjo,
1976; Samtleben and Bickert, 1990; Knappertsbusch and Brummer, 1995; Fagger-
bakke et al., 1994; Beaufort and Heussner, 1999). The basic approach used in most of
these studies (e.g., Beaufort and Heussner, 1999) is to calculate the surface area of the
coccolith, estimate an average thickness, and calculate the resultant volume making
some corrections for tube structures, etc. These estimates provide a useful starting
point, but they exclude several signi"cant species. In addition, estimates vary greatly
between the sources, errors are unquanti"ed, and the e!ect of size variation on volume
estimates has barely been discussed.
This paper presents new calculations of coccolith, and nannolith, volume for the
most abundant extant species. These estimates are based mainly on calculation of
coccolith volume from cross-sectional shape. This is a slightly complex technique, but
is the most accurate geometric approach possible. Discussion of the results focuses on
analysis of errors and the extent to which #ux rates can be derived in this way.

2. Material and methods

2.1. Material and microscopy

A set of sediment trap samples from the UK North Atlantic JGOFS 1989 station
(483N, 203W, 3000 m water depth) has been used here as a case study. Details of these
traps are given in Newton et al. (1994). The samples have been used to provide
estimates of coccolith length applicable to coccolith studies in this region, and to
provide a specimen set of coccolith counts to demonstrate the e!ect of converting
 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700 1681

species counts into carbonate mass distributions. 1/64 rotary splits were provided by
Dr.R. Lampitt (Institute of Oceanographic Sciences). Strew preparations were made
from these using 1 ml micropipette sub-samples, after homogenisation but without
special preparation techniques. Slides were counted by light microscopy with count-
ing of 10 "elds of view at ;1600, followed by extended counting of larger specimens.
All counts were converted initially into specimens per unit slide area and then into
#uxes (based on slide area, sub-sample size, split size, sampling duration and trap
opening size). Coccolith size measurements were carried out at ;1600 magni"cation
using a double-ruled eyepiece graticule, giving a resolution of 0.32 lm or, for the
smallest coccoliths, by using a digital image-capture system, as described by Young
et al. (1996).
The use of a pipette rather than a rotary splitter for the "nal sub-sampling may have
introduced sampling errors. In addition, #ocs were present in most samples, which
contained signi"cant numbers of coccoliths that were not possible to count. So, the
coccolith #ux estimates given for these samples have substantial associated errors.
Broerse et al. (2000) describe techniques for reducing these errors.

2.2. Coccolith volume calculation

For any given shape, volume is a cubic function of linear dimension, e.g., for spheres
<"4/3pr, for cubes <"l. Or, more generally, <"k l where k is a constant
 
dependent on the shape and l is a characteristic dimension. If l is maximum
length/diameter, then for a sphere k "p/6"0.52, and for a cube k "1.
 
If we assume that for a given coccolith species the shape is scale invariant (discussed
below), then volume determination can be separated into two stages: "rst determina-
tion of the shape constant k ; second determination of the size, l. As an additional step,

volume can be converted to mass by multiplying by the density of calcite
(2.7 g/cm"2.7 pg/lm).

2.2.1. Determination of k from a coccolith cross-section


Coccoliths possess a high degree of radial symmetry; hence volume can be cal-
culated from a cross-section parallel to the axis of radial symmetry. A minority of
coccoliths are circular, and for them calculation of volume from a cross-section can be
carried out as follows: (a) the thickness of the coccolith cross-section is measured at
each of n increments out from the axis of the cross-section; (b) for each increment the
volume is calculated as a hollow cylinder; and (c) these volumes are integrated (Fig. 1).

GL
<" t p[(r/(i#1))!r/i)], (1)
G
G
where < is the volume, r is the radius of the coccolith, and t is the thickness at r/i.
G
Most coccoliths, however, are elliptical rather than circular, so the equation needs
to be adjusted. In detail, the geometry of elliptical coccoliths is such that the width of
each concentric element or part of the coccolith is uniform around the coccolith and
so the ellipticity varies outwards. That is, coccoliths may be modelled as having the
1682 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700

Fig. 1. Calculation of the volume of a coccolith from its shape in cross-section. All the relevant information
for volume calculation from the complete coccolith (A) is contained in the cross-section (B). From this,
a plot of thickness against distance from the centre of the coccolith can be derived (C). For each incremental
distance from the centre the volume can then be calculated (D), based on a circular or elliptical cylinder as
appropriate. Graph D is thus a plot of volume distribution across the width of the coccolith.

geometry of a set of co-axial parallel ellipses, rather than similar ellipses (Young, 1989;
Young et al., 1996). Hence, for elliptical coccoliths, the equation needs to be modi"ed
to:

GL
<" t p[a/(i#1#q)a/(i#1)!(a/i#q)(a/i)], (2)
G
G
where a and b are the long and short axes of the coccolith, and q"a!b. For circular
coccoliths a"b; hence q"0, so Eq. (1) can be seen to be a special form of Eq. (2).
Image analysis programs provide a convenient means of implementing this type of
calculation, since they provide both the tools for measuring images such as cross-
sections and macro-programming languages suitable for of carrying out the calcu-
lations needed. The program used here is NIH-Image, a popular image analysis
package for Apple MacIntosh. This is a public domain program produced by the US
National Institutes of Health and available on the Internet at http://rsb.info.nih.gov/
nih-image/. A Windows version, Scion Image, is available, as freeware, from Scion
Corporation at http://www.scioncorp.com.
 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700 1683

An NIH-Image macroprogram has been written to calculate volumes of rotation

from cross-sections. Given a digitised cross-section (Fig. 1B) and axial ratio as inputs,
the program measures and displays thickness as a function of distance from the axis of
symmetry (Fig. 1C) calculates the implied volume, and displays the result (Fig. 1D).
The digitised section is a simple binary (black on white) object with the symmetry axis
vertical. The program measures the cross-section thickness at each increment, t , by
G
counting the numbers of pixels in each column of the object. Volume calculation is
based on the equations given above. Copies of the program to allow these calculations
can be obtained from the senior author.
An alternative approach would be to use a 3D CAD package to generate a
solid of rotation from a cross-section. This is a slower and less #exible approach,
and cannot easily incorporate accurate ellipticity corrections, but it does not
require any programming since most CAD packages can automatically calculate
volumes.

2.2.2. Method of obtaining cross-sections

The prime input needed for volume determination is an accurate cross-section.
These are di$cult to obtain since coccoliths are normally seen in plan or oblique view,
so problems in cross-section construction constitute the main constraint on accurate
volume estimation.
Light microscopy (LM) can be used to obtain cross-sections * with careful
searching specimens lying on edge often can be found and, if not, then mobile mounts
can be used to tilt individual specimens (e.g., Gartner, 1969; Romein, 1979). We used
both techniques, combined with digital image capture, to obtain computer images of
specimens. Informative cross-sectional views can be obtained this way, but the edges
of the specimen are usually indistinct which introduces signi"cant uncertainty into the
cross-sections, especially of small specimens.
With scanning electron microscopy (SEM), cross-sections can be only obtained
directly from fortuitously broken specimens. More generally, it is necessary to use side
views and attempt to reconstruct the likely cross-section from them. In addition, plan
view SEM images are ideal for determining the axial ratios of elliptical coccoliths and
for measurements on the relative width of di!erent cycles. The technique used in both
cases was to digitally scan useful SEM images, both from our own collections and
from the literature.
For both image types digital images were imported into a vector-based graphics
program, then cross-section outlines were drawn and copied to NIH-Image for
volume calculation. For a few common coccolith taxa several cross-sections were
produced using di!erent techniques in order to investigate the range of uncertainty,
and to develop a general technique. From this experience, it was found that the
following procedure was most e!ective; it was then used to reconstruct single cross-
sections of several less common species (Fig. 2): (1) Plan view electron micrographs
were used to determine the relative widths of the di!erent parts of the coccolith pro"le.
(2) Light micrograph cross-sections were used to constrain the general proportions of
the coccolith pro"le. (3) SEM images of broken or tilted specimens were used to
determine the thickness of individual elements.
1684 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700

Fig. 2. Cross-section reconstruction. Illustration of how SEM and LM data can be combined. The
coccolith is of Neosphaera coccolithomorpha. The LM pro"le is used to constrain the general shape of the
cross-section, whilst the plan view SEM provides relatively precise indication of the relative width of the
di!erent parts of the coccolith.

3. Results

3.1. Volume determinations

Basic results are given in Table 1 for all species measured; these consist of the range
of k values determined and a recommended value of k for each species. This k value
  
is not a simple arithmetical mean of the obtained values since the data quality varied,
but rather an estimate of an appropriate value after some experimentation into the
e!ect of slight variations in pro"le, shape, etc. on k values. In general, independently

produced pro"les and experiments with slight alterations to pro"les suggested that
k values could be derived with an accuracy of about $20%. This degree of

uncertainty is inevitable due both to di$culties in creating an accurate cross-section
and to intrinsic variability.
Fig. 3 shows for each species a cross-section, which gives the recommended value of
k . Table 1 also gives a size range for the species, and a volume range, based on the

k value. Finally, a typical mean size is given and resultant estimates of typical size and

mass (N.B. both size range and mean sizes will vary between samples as discussed
below.) The size ranges and mean sizes are predominantly based on the JGOFS
sediment trap samples.
 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700 1685

Fig. 3. Coccolith pro"les. Coccolith pro"les with the values of k determined here (Table 1).


Notes below discuss variations in approach required for particular species.

Emiliania huxleyi: The slits between elements in E. huxleyi coccolith shields were
accounted for by thinning the relevant parts of the pro"les. Several di!erent values of
k are given for E. huxleyi since it shows important variation in degree of calci"cation

and pro"le. The dominant form, type A (Young and Westbroek, 1991), shows a high
degree of variation in degree of calci"cation (Young, 1994), re#ected in variable
closure of the central area and variable thickness of the shield elements. Our pro"le
reconstructions suggest this causes a four-fold variation in k . This appears to be an

unusual feature of E. huxleyi; other coccoliths do not obviously show comparable
 1686

Table 1
Our estimates of shape constant, k , for di!erent species based on analysis of cross-pro"le shape

Species No. of Range of Recom- One- Length Length Mean Volume Volume Mass at
sections k values mended dimension, data, liths range length range at mean mean
 
reconstructed value if not measured (lm) (lm) (lm) length length
length (lm) (pg)

Acanthoica sp., body coccolith 1 0.033 0.03 Estimate 1}2 1.5 0.03}0.24 0.1 0.3
Calcidiscus leptoporus 7 0.068}0.103 0.08 257 5}11 7 10}106 27.4 74.1
Ceratolithus cristatus 1 0.097 0.1 Width Estimate 4}10 9 6.4}100 72.9 196.8
Coccolithus pelagicus 4 0.04}0.07 0.06 481 6}16 9.6 13}246 53.1 143.3
Coronosphaera binodata 2 0.093}0.094 0.09 Estimate 3}4.5 3.5 2.4}8.2 3.9 10.4
Coronosphaera mediterranea 2 0.063}0.075 0.07 Estimate 3}5 4 1.9}8.8 4.5 12.1
Discosphaera tubifera 8 0.053}0.087 0.07 Trumpet Estimate 1.5}2.5 2 0.24}1.1 0.6 1.5
width
Emiliania huxleyi type A 4 0.016}0.021 0.02 55 2.5}4.5 3.5 0.31}1.8 0.9 2.3
normally calci"ed
J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700

Emiliania huxleyi type A Adjusted from normally 0.04 111 2.5}4.5 3.5 0.63}3.6 1.7 4.6
overcalci"ed calci"ed form
Emiliania huxleyi type A Adjusted from normally 0.01 Estimate 2.5}4.5 3.5 0.16}0.09 0.4 1.2
undercalci"ed calci"ed form
Emiliania huxleyi type B 3 0.014}0.028 0.02 Estimate 4}5 4 1.3}2.5 1.3 3.5
Florisphaera profunda 9 0.03}0.06 0.04 Estimate 2}5 2.5 0.3}5 0.6 1.7
Gephyrocapsa oceanica 14 0.037}0.060 0.05 Estimate 3.5}5 4.5 2.14}6.2 4.6 12.3
Gephyrocapsa muelerae Adopted from G. oceanica 0.05 46 3}4.5 3.9 1.4}4.6 3.0 8.0
Gephyrocapsa ericsonii Adopted from G. oceanica 0.05 Estimate 2.5}3.5 3 0.8}2.3 1.4 3.6
Helicosphaera carteri Adjusted from C. pelagicus 0.05 63 8}12 10 27}86 50.0 135.0
Neosphaera coccolithomorpha 1 0.016 0.015 Estimate 7}10 8 5}15 7.7 20.7
Oolithotus fragilis Adjusted from C. leptoporus 0.07 23 5}8 8 9}36 35.8 96.8
Rhabdosphaera clavigera 6 0.015}0.026 0.025 Spine length 26 6}12 10 5}43 25.0 67.5
Rhabdosphaera stylifera 3 0.011}0.017 0.015 Spine length Estimate 6}12 10 3}26 15.0 40.5
Scyphosphaera apsteinii 3 0.15}0.25 0.2 Width in Estimate 8}12 10 100}345 200.0 540.0
pro"le
Small Syracosphaera species 4 0.015}0.024 0.015 Estimate 1}3 1.5 0.015}0.4 0.1 0.1
Syracosphaera pulchra 4 0.028}0.033 0.03 36 4}7 5.5 1.9}10 5.0 13.5
Thoracosphaera heimii 6 0.16}0.22 0.2 10 10}18 13 200}1150 439.4 1186.4
Umbellosphaera tenuis 2 0.012}0.016 0.015 Estimate 5}8 6 1.9}7.7 3.2 8.7
U. irregularis Adjusted from U. tenuis 0.01 Estimate 5}8 6 1.25}5.1 2.2 5.8
Umbilicosphaera sibogae var. 4 0.054}0.084 0.06 Estimate 3}5 6 1.6}7.5 13.0 35.0
foliosa
Umbilicosphaera sibogae var. 6 0.043}0.067 0.05 Estimate 3}4 5 1.35}3.2 6.3 16.9
sibogae

N.B. volume"k l. For most species one or more cross-sections were reconstructed, yielding the range of k values and a recommended value. In other cases, as
 
indicated, k values either have been adopted from similar species without change or adjusted from similar species with some compensation for change in degree

of calci"cation. Length data: Estimate-values are approximate, based on literature review and measurement of a few SEMs; otherwise number of specimens
measured in LM from the JGOFS sediment trap samples. In any detailed study, locally appropriate mean lengths should be used. Length and volume ranges are
given to highlight the very great intraspeci"c variation in volume.
J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700
1687
1688 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700

primary variation. Type B E. huxleyi coccoliths appear less heavily calci"ed but are
signi"cantly higher in cross pro"le, and cross pro"les gave k values comparable to

those of normally calci"ed type A.

Gephyrocapsa: Detailed reconstructions were made on G. oceanica specimens. Bridge

volume was calculated separately based on shape in pro"le and thickness; these
calculations suggested the bridge forms 10}15% of total coccolith volume. The other
Gephyrocapsa species have similar cross-sections, so the same k values are recommen-

ded for these species.

Helicosphaera carteri: The k value given is based on that of Coccolithus pelagicus


since H. carteri coccoliths have a helical morphology, which cannot easily be
modelled. The value is reduced from that of C. pelagicus by 20% since the coccoliths
are somewhat less thick.

Oolithotus fragilis: O. fragilis is similar to Calcidiscus leptoporus but with a smaller,

o!-centre, proximal shield. The k value given was derived by taking a typical

C. leptoporus section and reducing the proximal shield size.

Umbellosphaera: Detailed reconstructions were made on U. irregularis specimens; for

U. tenuis a reduced k value is recommended based on an estimate of the coccolith

thickness in this species.

Florisphaera profunda: The k value is based on a simple model as a lath of uniform


thickness with shape and size determined from SEM and LM observations.

Thoracosphaera heimii: The k value is based on LM measurements of the inner and


outer diameter of 12 spheres with an estimate of 20% porosity.

Ceratolithus cristatus: The k value is based on measurement of side and plan view

SEMs of a single specimen. This was divided into several of sub-parts (keels, apical
area, left arm, and right arm); the areas of these were determined in NIH Image and
estimates of their mean thickness applied. The k value has been based on the

maximum width of the ceratolith rather than the arm length since ceratoliths often
have long delicate arms that contribute little to the total volume.

Coccosphere volume calculation: Coccospheres of Coccolithus pelagicus are common in

the JGOFS sediment trap samples, and two independent techniques were used to
determine their volumes. (a) The number of coccoliths per coccosphere was estimated
from SEM images (10 coccospheres from these samples) and a volume estimated using
the mean coccolith volume calculated for these samples. Based on 16 coccoliths per
coccosphere, each with a volume of 132 lm, this yielded a value of 2100 lm. (b) The
inner and outer diameters of 33 coccospheres were measured in the LM, their volumes
calculated and averaged. This yielded an average volume of 3920 lm. Assuming that
 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700 1689

this volume is 50% "lled by coccoliths reduces this value to 1960 lm. These values
are strikingly close, suggesting that either technique may be used, as convenient.

3.2. JGOFS sediment trap sample analysis

The di!erence between assemblage composition in terms of numbers of specimens

(Fig. 4, upper) and composition in terms of carbonate content (Fig. 4, middle) is
striking. Emiliania huxleyi and Gephyrocapsa muellerae dominate the coccolith counts.
In terms of mass, however, these species make a rather low contribution, owing to the
much greater per specimen mass of species such as Coccolithus pelagicus, Thoracospha-
era heimii and Calcidiscus leptoporus.
The bottom graph in Fig. 4 gives counts converted into particulate inorganic
carbon (PIC) #ux, and the total PIC #ux as determined independently by Newton et
al. (1994) by chemical means. The coccolith PIC #ux apparently constitutes 30}80%
of the total PIC, which is close to expectation. Indeed, the correlation of the results is
a remarkable vindication of the overall technique. In addition, the data indicate that
the peak in coccolith PIC values is largely a result of the contribution of Coccolithus
pelagicus; other species show little variability.

3.3. Uncertainties in volume calculation

3.3.1. Allometric growth

The e!ect of size has assumed that shape does not change signi"cantly with size,
which is an over-simpli"cation. Large and small coccoliths of a given species are not
simply scaled-up versions. In most species the strongest allometric e!ect in coccolith
growth is an increase in the number of elements with size; this, however, does not alter
the cross-sectional pro"le (Young, 1989). Other consistent allometric e!ects have not
been documented widely. The most important question is whether the height of
coccolith and thickness of elements increases in proportion to coccolith length. It was
not possible to collect enough data to analyse this quantitatively, but available
evidence from cross-section examination and birefringence changes suggests that
height and thickness increase in line with planar dimensions.

3.3.2. Coccolith geometry model

As described above, the values of k given here were based on a parallel ellipse

model of coccolith geometry. This is the most appropriate model to use for most
coccoliths (Young, 1989; Young et al., 1996); however, it has the disadvantage that
calculating values for di!erent axial ratios is only possible via a complete recalcula-
tion from the coccolith cross-section. A simple approximation would be to assume
that the volume of an elliptical coccolith would equal the volume of a circular
coccolith of similar width multiplied by the axial ratio (this is equivalent to assuming
a similar ellipse model of coccolith geometry). In some cases it may be useful to
produce approximations on this basis; so, a sensitivity analysis has been carried out.
For "ve typical coccolith cross-sections accurate volume estimations based on the
parallel ellipse model were computed and also simple estimates based on the similar
1690 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700
 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700 1691

ellipse model. The di!erence in estimates between the two models can be signi"cant
('20%) if the volume is concentrated near the edge or centre of coccoliths. However,
for coccoliths with a more uniform distribution of volume across the coccolith, such as
most placoliths, and for the normal range of axial ratios (1.0}1.4), the e!ect of choice of
geometrical model is usually slight ((10%). Hence, corrections for axial ratio
variation based on the simpler model usually should not introduce large errors, and
certainly are preferable to not making any correction.

3.3.3. Errors from length variation

Coccolithophorids and the coccoliths they produce, like any other organisms, vary
in size as a result of both genotypic variability and varying growth response to
di!erent ecological conditions. The most detailed results are available from Emiliania
huxleyi (e.g. Young and Westbroek, 1989; Bleiswijk et al., 1991; Young, 1994; Paasche
et al., 1996; Batvik et al., 1997; Young unpubl. data). Typically a monoalgal culture of
a single E. huxleyi strain will produce mature coccoliths varying in size by about 40%
(e.g., from 2.5 to 3.5 lm with a normal size frequency distribution. Varying ecological
growth conditions will extend the total variability somewhat and also can shift mean
size, by a maximum of about 30% (e.g., 3}4 lm).
Genotypic variability can increase this total variability considerably. Young and
Westbroek (1989) recognised three varieties of E. huxleyi, types A, B, and C, with
typical size ranges of: 2.5}4, 4}5.5 and 2}3.5 lm, respectively. Medlin et al. (1996)
consider these three types of distinct species * E. huxleyi, E. pujosae and E. kleijneae,
respectively, however, di!erentiation is di$cult, and despite considerable interest in
the species few workers have found it practicable to di!erentiate them consistently.
Hence assemblages of E. huxleyi (sensu lato) coccoliths can have sizes ranging from
about 2 to 5.5 lm and mean sizes ranging from about 2.5 to 5 lm, with genotypic
variation being the single most important cause of size variation. This two-fold
variability in coccolith length is liable to correspond to an eight-fold variability in
volume, which is plainly signi"cant in terms of #ux estimation.
Other species are generally less well studied than E. huxleyi, but available evidence
indicates that most common species display comparable degrees of size variation and
that it is mainly genotypically driven (e.g., Kleijne, 1993; Knappertsbusch et al., 1997;
Bollmann, 1997). Noteworthy examples of size variation in the JGOFS samples
include Coccolithus (coccolith sizes range from 6.5 to 16.5 lm with two discrete size
de"ned sub-types, based on LM measurement of 481 coccoliths), and Calcidiscus
(coccolith sizes range from 5 to 11 lm but without obvious sub-types, based on LM
measurement of 257 coccoliths).

䉳
Fig. 4. Coccolith count and #ux data from the JGOFS sediment trap. All data are from JGOFS sediment
trap samples collected from 473N 203W, 3100 m in early summer 1989. Top, assemblage composition in
terms of % abundance of di!erent species by coccolith count. Centre, assemblage composition in terms of
% mass contribution by di!erent species. Bottom, absolute coccolith #uxes, in comparison to total
calculated particulate inorganic carbon (PIC) #ux. (N.B. per coccolith PIC #ux"0.12;mass #ux; based on
assumption that coccoliths are formed of pure CaCO ).

1692 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700

Clearly, it is not reasonable to assume that a single mean volume can be universally
assigned to each coccolith species. For instance, a volume calculation for Calcidiscus
leptoporus based on samples from these mid-latitude North Atlantic samples should
not be applied to equatorial Paci"c samples without checking that the coccoliths are
of similar size. In most studies of modern material, it should be possible to use a single
size calibration throughout the study, but obviously if a key species varies signi"cantly
in size between samples, this should be taken into account. For geological studies, this
may not be a reasonable assumption since numerous species show signi"cant size
variation through time.
The potential errors due to size variation (easily up to 10;-volume variation) are
larger than other sources of potential error, so calibrations should be made for at least
the most volumetrically important species. This calibration can be made easily and
rapidly by measuring about 50 specimens of coccoliths of the given species by light
microscopy using an eyepiece graticule. This should generally provide a size estimate
with an error of about 5}10%, and so a volume estimate error of 15}30%.

3.3.4. Choice of size for volume calculation

For maximum accuracy in determining the speci"c volume of a species, the mean
volume should be calculated rather than the volume of the coccolith of mean linear
size, i.e.


k .l l 
<M "  not <M "k . .
n  n

If a simple mean length is used, then the volume will be undercalculated, the extent
depending on the distribution of values. For normal distributions, the size of the error
will be a function of the relative magnitude of the standard deviation and the mean.
Typical values are given in Table 3. The e!ect is less than 10% for standard deviations
of around 0.2; mean, a typical value in coccolith populations, so using a simple mean
will probably not result in signi"cant changes in volume estimates. Correction for this will
only be justi"ed if the size structure of the population has been worked out with particular
care. With a bimodal or skewed population, larger errors could be introduced.

3.3.5. Volume to mass conversion

We have converted volumes to masses using a density of 2.7 g/cm ("2.7 pg/lm).
This seems reasonable since chemical analyses have typically shown that coccoliths
are formed of very pure calcite (e.g., Faggerbakke et al., 1994) without a substantial
intracellular organic phase. In addition, SEM observations of fractured surfaces show
no evidence of porosity in coccoliths.

4. Discussion
4.1. Comparison of results

Table 2 provides a review of other authors mass estimates compared to ours. In

most cases the authors have provided a mass or volume estimate together with some
 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700 1693

data on coccolith size which enabled back calculation of k values from their data. In

a few cases no size data were provided, so we had to infer likely size values in order to
calculate k values. As might be expected, the mass estimates vary signi"cantly

between di!erent authors and between our data. Comparison of the mass or volume
estimates of di!erent authors with ours (Table 1) suggests a disturbingly wide uncer-
tainty. However, the values of k show much lower variation, typically estimates vary

by only 10}20%, in line with our estimate that this was the likely limit of reliability in
k estimation. The variation in mass estimates thus primarily re#ects the fact that

mass estimates are highly dependent on the adopted coccolith size. The similarity of
k values is encouraging, suggesting that di!erent methods of estimating volume from

a given coccolith size yield broadly comparable results. Again however, the compari-
son of these estimates emphasises the need for accurate size calibration. A few species
show signi"cant variations in k estimates:


E. huxleyi; published mass and implicit k estimates are highly variable. This is

probably a re#ection of the unusually (? uniquely) variable degree of calci"cation of
this species. Low values of Paasche (1962) and Linschooten et al. (1991) are from
coccoliths grown in culture, which almost always are under-calci"ed. The low value of
Faggerbakke et al. (1994) was from mesocosm experiments, but these coccoliths were
mainly under-calci"ed (Young, 1994). By contrast, the estimate of Samtleben and
Bickert (1991) was based on over-calci"ed high-latitude specimens.

Thoracosphaera heimii: Knappertsbusch and Brummer (1995) quote a mass of

7.56;10\ g based on diameter of 15.5 lm, a wall thickness of 1 lm and a 6 lm
diameter aperture. This mass and diameter yield a k , value which is substantially

higher than ours, 0.75 vs 0.20. The value of 0.75 is plainly in error since it is rather
higher than that for a solid sphere (0.52). Recalculation from the size data they quote
suggests they misquoted the calculated mass, which should have been 0.756;10\ g.

Umbellosphaera tenuis: the k value from Beaufort and Heussner (2000) is substantially

higher than ours 0.076 vs 0.015. This is primarily due to their adopting a thickness for
the distal shield of 0.75 lm, which appears excessive.

Typical small coccolith: Honjo (1976) produced one of the most widely used "gures for
coccolith size, based on an `average coccolitha. Using a length of 5 lm and width of
3 lm, he calculated a volume of 22 lm, which is improbably high for a coccolith of
this size (k "0.176), and a weight of 8 pg. These values are mutually inconsistent, (he

appears to have divided instead of multiplied by density). The "nal "gure of 8 pg is
thus not logically derived, but curiously is not a bad estimate for the small coccoliths
that numerically dominate coccolith #uxes. Hence, the practice of using this estimate
as a standard value for coccoliths for which accurate estimates were not available (e.g.,
Knappertsbusch and Brummer, 1995) should not have caused gross errors. However,
if the values given here are adopted, then the residual category of small coccoliths is
mostly made up of much smaller coccoliths. The small coccolith volume given here
Table 2
Comparison of estimates of mass, volume and shape constant calculated here and by other workers
1694

Species Mass Mass Volume Length k Source


CaCO Ca (lm) (lm) ("vol/l)

(pg) (pg)

Coccosphaerales
C. pelagicus 151.2 60.5 56.0 10.35 0.051 Beaufort and Heussner (1999)
C. pelagicus 130.0 52.0 48.0 10 0.048 Samtleben and Bickert (1990)
C. pelagicus large (*10.5 lm) 398.6 159.4 147.6 13.5 0.060 This study
C. pelagicus small ((10.5 lm) 99.5 39.8 36.8 8.5 0.060 This study
C. pelagicus mixed pop. 355.9 142.4 131.8 13 0.060 This study
C. leptoporus large 164.2 65.7 60.8 9.6 0.069 Beaufort and Heussner (1999)
C. leptoporus small 22.6 9.0 8.4 4.3 0.105 Beaufort and Heussner (1999)
C. leptoporus 57.0 22.8 21.0 7 0.061 Knappertsbusch (pers. comm.)
C. leptoporus 74.1 29.6 27.4 7 0.080 This study
U. sibogae 16.0 6.4 5.9 4.1 0.086 Beaufort and Heussner (1999)
U. sibogae sibogae 18.6 7.4 6.9 5 0.055 This study
U. sibogae foliosa 35.0 14.0 13.0 6 0.060 This study
O. fragilis 96.8 38.7 35.8 8 0.070 This study
N. coccolithomorpha-large 40.5 16.2 15.0 10 0.015 This study
Prinsiales
E. huxleyi 2.9 1.2 1.1 3.1 0.036 Beaufort and Heussner (1999)
E. huxleyi 3.0 1.2 1.1 3.2 0.034 Samtleben and Bickert (1991)
E. huxleyi 1.4 0.6 0.5 3.2 0.015 Paasche (1962)
E. huxleyi 1.7 0.7 0.6 3.8 0.011 Faggerbakke et al. (1995)
E. huxleyi 0.6 0.2 0.2 3 0.008 Linschooten et al. (1991)
E. huxleyi var A-overcalci"ed 4.6 1.9 1.7 3.5 0.040 This study
J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700

E. huxleyi var A-normally calci"ed 2.3 0.9 0.9 3.5 0.020 This study
E. huxleyi var A-undercalci"ed 1.2 0.5 0.4 3.5 0.010 This study
E. huxleyi var B-normally calci"ed 3.5 1.4 1.3 4 0.020 This study
ericsonii 5.8 2.3 2.2 3.21 0.065 Beaufort and Heussner (1999)
G. oceanica 25.7 10.3 9.5 5.35 0.062 Beaufort and Heussner (1999)
G. oceanica 18.0 7.2 6.6 5 0.053 Knappertsbusch (pers. comm.)
G. oceanica 16.9 6.8 6.3 5 0.050 This study
G. muellerae 8.0 3.2 3.0 3.9 0.050 This study
G. ericsonii 3.6 1.5 1.4 3 0.050 This study

Rhabdosphaerales
Acanthoica 0.3 0.1 0.1 1.5 0.030 This study
R. clavigera 67.5 27.0 25.0 10 0.025 This study
R. stylifera 40.5 16.2 15.0 10 0.015 This study
D. tubifera 1.5 0.6 0.6 2 0.070 This study
U. tenuis 23.9 9.5 8.8 5 0.071 Beaufort and Heussner (1999)
U. tenuis 8.7 3.5 3.2 6 0.015 This study
U. irregularis 5.8 2.3 2.2 6 0.010 This study
Syracosphaerales
Syracosphaera sp. 12.1 4.9 4.5 5.21 0.032 Beaufort and Heussner (1999)
S. pulchra 16.5 6.6 6.1 5.85 0.031 Beaufort and Heussner (1999)
S. cf. mohleri 4.4 1.8 1.6 2.7 0.083 Beaufort and Heussner (1999)
S. pulchra 16.0 6.4 5.9 6 0.027 Knappertsbusch and Brummer (1995)
S. pulchra 13.5 5.4 5.0 5.5 0.030 This study
Syracosphaera - small 0.1 0.1 0.1 1.5 0.015 This study
Coronsphaera binodata 10.4 4.2 3.9 3.5 0.090 This study
C. mediterranea 12.1 4.8 4.5 4 0.070 This study
Zygodiscales
P. japonica 70.1 28.0 26.0 8.2 0.047 Beaufort and Heussner (1999)
P. discopora 65.9 26.4 24.4 7.9 0.050 Beaufort and Heussner (1999)
Scyphosphaera apsteinii 540.0 216.0 200.0 10 0.200 This study
H. carteri 142.8 57.1 52.9 9.1 0.070 Beaufort and Heussner (1999)
H. carteri 135.0 54.0 50.0 10 0.050 This study
Nannoliths
J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700

B. bigelowii 85.5 34.2 31.7 7.1 0.088 Beaufort and Heussner (1999)
F. profunda 5.3 2.1 2.0 4.2 0.027 Beaufort and Heussner (1999)
F. profunda 1.3 0.5 0.5 2.5 0.030 This study
Ceratolithus cristatus 196.8 78.7 72.9 9 0.100 This study
1695
 1696

Table 2 (continued)

Species Mass Mass Volume Length k Source


CaCO Ca (lm) (lm) ("vol/l)

(pg) (pg)

Calcareous dino6agellate
T. heimii 1186.4 474.6 439.4 13 0.200 This study
T. heimii 7560.0 3024.0 2789.7 15.5 0.749 Knappertsbusch and Brummer (1995)
Typical small coccolith
Small coccolith 2.6 1.0 0.9 3 0.035 This study
Average coccolith 59.6 23.8 22.0 5 0.176 Honjo 1976 (from quoted volume)
Average coccolith 8.0 3.2 3.0 5 0.024 Honjo 1976 (from quoted mass)

(Italicised values of length are my estimates, italicised values of k are calculated from length and volume data). For our data the mass and volume estimates are

calculated from the shape factor based on a mean size derived, in most cases from the JGOFS samples. The literature values are mass and/or volume estimates as
given in the reference and k values calculated here based on either a quoted length or an inferred likely length (italicised values). See text for discussion of

discrepancies between values calculated here and by other workers.
J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700
 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700 1697

Table 3
Calculated values of mean of cubes/cube of means for normally distributed populations with varying values
of standard deviation/mean

SD/mean Mean of cubes/cube of means

0.00 1.00
0.05 1.01
0.10 1.03
0.15 1.07
0.20 1.12
0.25 1.19
0.30 1.27
0.35 1.35
0.40 1.43

Volume calculations ideally should be based on the mean of cubed lengths rather than the cube of mean
lengths, but, as this table shows for populations with moderate variation in length (SD/mean(0.2), the
variation between these values is low enough to be ignored.

(0.9 lm, 2.5 pg) is a crude estimate, intended to provide a reasonable "gure this
category.
Identifying calculation errors in some published values highlights the need for
checking all calculations. One way to do this is to calculate k values. For coccoliths

k values usually fall in the range 0.01}0.1, so values outside this range should be

double-checked.

4.1.1. Estimation of relative yux contribution and ecological role

As shown by the JGOFS data (Fig. 4), coccolith counts and mass estimates provide
radically di!erent impressions of the relative importance of di!erent species. For
estimation of relative #ux contributions, conversion into mass estimates is obviously
essential. It is also worth noting that mass estimates may be more appropriate than
count estimates for ecological interpretation. Owing to the range of size variation and
the range in numbers of liths per cell, the ecological relevance of simple coccolith
counts is rather questionable. Mass estimates are also certainly subject to reserva-
tions; in particular the ratio of coccolith calcite to cell biomass is variable between
species (at least two}three-fold). Nonetheless, mass estimation may be worth inves-
tigating to see if it does yield more meaningful information than other count types.
Mass contributions for instance, may, be useful in palaeoecological and palaeoceano-
graphic interpretations of changes in nannofossil assemblage composition. This is
particularly so in the Quaternary where there is an extremely wide range of coccolith
sizes, with numerically abundant small species (especially Gephyrocapsa spp.,
Emiliania huxleyi and Florisphaera profunda) and less abundant large species (e.g.,
Coccolithus pelagicus, Calcidiscus leptoporus). Many authors have used separate
counts of small and large species in order to avoid losing data from the large species
(e.g., Okada, 1992); using mass calibrations may prove a useful way to compare data
from the two groups. In fossil material variable preservation will introduce further
1698 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700

errors, so any palaeo#ux estimates should be interpreted with restraint. Nonetheless,

we believe that quantifying per species mass #uxes may provide useful new perspect-
ives and help constrain hypotheses.

4.2. Limitations on use in sediment trap work in terms of total yux estimation

As explained above, estimates of volume are liable to contain errors of about 20%
due to uncertainties in cross-section reconstructions, 15}30% due to errors in length
estimate, and around 5}10% due to factors such as allometric growth and geometric
model. Therefore, coccolith volumes are likely to contain errors of around 40}50%. In
addition, estimates of #uxes are liable to signi"cant errors due to incomplete break-
down of pellets and marine snow, counting errors, and problems in accurately
splitting samples to the small volumes needed for coccolith analysis. These factors
have attracted much attention by specialists looking at sediment trap samples, but
nonetheless certainly still introduce signi"cant additional uncertainties. So any esti-
mates of coccolith #ux based on species counts and volume estimates inevitably will
have substantial errors associated with them. The sediment trap data given here (Fig. 4)
are close enough to the total PIC value to have reasonable con"dence in it, but the
inherent errors mean that detailed analyses of variations in contribution to the #ux are
tenuous. Hence, alternative approaches for calculating total coccolith #ux should be
used if possible; for instance, calculations based on size fractionation of the carbonate.

5. Conclusions

1. Coccolith mass can be expressed as m"2.7k l


2. For most species a single "gure for the shape factor, k , can be given with

a reliability of approximately $20%. Between species k varies by about one

order of magnitude, and separate values per species should be adopted.
3. Values of k are given here based on a relatively sophisticated calculation methodo-

logy; however, simpler calculation methodologies give broadly comparable results.
4. Size variation has a much greater e!ect than shape variation in controlling
coccolith volume } within a single species, two}three-fold size variation is common,
resulting in 8}27-fold mass variation. Between common species size varies by an
order of magnitude and so mass by three orders of magnitude, i.e., 1000-fold.
5. To optimise #ux calculation results, it is essential that the size range of at least the
most volumetrically abundant coccoliths in the material be investigated. Using
a single mass estimate per species for all samples, even for modern material, will
result in substantial avoidable errors. For many modern species, two-fold variation
in mean size is likely between di!erent environments, resulting in eight-fold
variations in volume. Measuring the actual size range in the sample should reduce
this error to about 5}10% in length, 15}30% in volume. Size calibration is not
particularly time-consuming and should be a routine part of #ux studies.
6. Even if considerable care is taken, the combined uncertainties in k and size are

likely to result in errors of $50% when species accumulation rates are converted
 J.R. Young, P. Ziveri / Deep-Sea Research II 47 (2000) 1679}1700 1699

into speci"c #ux rates. Additional errors will be introduced by counting problems,
particularly if pellets or clumps of coccoliths are present. So, considerable care
should be taken in interpreting such data and in comparing results with data from
other groups, which are quite likely to have similar sized errors.
7. Notwithstanding the uncertainties in absolute values, #uxes can provide a valuable
new perspective for the study of coccolithophore ecology.

Acknowledgements

We are grateful to Richard Lampitt for providing the JGOFS samples used here.
Luc Beaufort and Harald Andruleit gave careful reviews of the manuscript and made
many valuable suggestions. The work was completed as part of the EC TMR project,
Coccolithophorid Evolutionary Biodiversity and Ecology Network CODENET, and
is a contribution of the project.

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