Changes in morphology during ontogeny can have profound
impacts on the physiology and biology of a species. Studies of ontogenetic
disparity through time are rare because of the lack of preservation of
developmental stages in the fossil record. As they grow by incremental
chamber accretion and retain evidence of growth in their shell, planktic
foraminifera are an ideal group for the study ontogenetic disparity through
the evolution of a higher taxon. Here, we quantify different developmental
stages in Jurassic foraminifers and infer the evolutionary implications of
the shape of these earliest representatives of the group. Using a Zeiss Xradia
micro-CT scanner, the development of
Disparity refers to the morphological variability within a taxon. Studies of disparity commonly quantify morphospace within and between taxa using adult specimens (e.g. Foote, 1993; Ciampaglio et al., 2001). This focus on adult specimens creates a sample bias that limits the efficacy of the approach by excluding developmental disparity. Fewer studies consider the influence on disparity of ontogenetic change both within taxa and over time (McNamara, 1986; Foote, 1993; McNamara and McKinney, 2005; Gerber et al., 2008) often limited by the lack of complete developmental sequences to perform the analysis.
Planktic foraminiferal morphology has been studied for decades to assess changes in their diversity through time (Ezard, 2011) with applications in biostratigraphy to environmental reconstructions (Perch-Nielsen et al., 1985; Kucera, 2007). All planktic foraminifers possess a calcareous, chambered test (Gradstein et al., 2017a) composed of aragonite or calcite (BouDagher-Fadel et al., 1997). Growth occurs through the addition of chambers (Brummer et al., 1987; Caromel et al., 2016), which are preserved in the adult test, enabling analysis of developmental disparity in a similar way to larger invertebrates such as ammonoids (Bucher et al., 1996). Ontogenetic stages from juvenile to neanic to adult are categorized through changes in morphology (Brummer et al., 1987; Caromel et al., 2016). The adult stage is defined by the maturation of the wall texture and a decline in growth rate. Neanic and juvenile stages are more difficult to differentiate due to the poor preservation of earlier chambers. Several theoretically possible morphologies (Berger, 1969; Tyszka, 2006) are not expressed in their adult morphology.
Locality map of Jurassic specimens. The Tojeira Formation is
indicated in blue, and Gnaszyn quarry in red. Further locality information
provided in Gradstein et al. (2017a). Map taken from
While modern foraminiferal disparity has been studied recently (Brummer et al., 1987; Caromel et al., 2016; Schmidt et al., 2016), few studies assess ontogeny in Mesozoic planktic foraminifers (Huber, 1994). Foraminifers are morphologically conservative (Brummer et al., 1986), repeating their same bauplan over and over again after every extinction (Cifelli, 1969). What is unclear is the amount of change in developmental disparity hidden in this conservative morphology. Planktic foraminifers evolved from a benthic ancestor in the Jurassic (Toarcian) Tethys Ocean (BouDagher-Fadel et al., 1997; Gradstein, 2017). Much of the first 40 million years of their evolution is fragmentary due to their small size and aragonitic shells (Gradstein et al., 2017a). The timing and cause of the change in mineralogy from aragonite to calcite is unknown, although it is believed to be post-Jurassic (Gradstein et al., 2017a).
Descriptions have historically relied on poor-quality preservations and acid
treatment, which removes many of the taxonomically important features
(Gradstein
et al., 2017a). Studies of planktic foraminifera development to date have
used a variety of tools, the easiest and most accessible being light
microscopy and scanning electron microscopy (SEM)
(Brummer et al., 1987). These
techniques can be informative for descriptive characteristics such as
overall morphology (in light microscopy) and wall structure (in SEM) but are
less useful for studying ontogenetic changes. No studies of the disparity
within the earliest members of the group exist due to their very small size
(generally less than 250
Here we analyse the ontogenetic growth patterns of four species of foraminifers using the recently developed technique of micro-CT scanning to reconstruct the developmental history of Jurassic planktic foraminifers and assess if their growth patterns through their development differ from modern foraminifers.
Four adult specimens from the Jurassic have been selected (Fig. 1) so that
complete reconstructions of their ontogeny could be made. Previous work has
shown that the developmental trajectories are conservative and highly
reducible between specimens of the same species
(Caromel et al., 2016). The oldest specimens,
2-D scans and 3-D isosurface reconstructions of Jurassic specimens
from Avizo 8.0 (spiral, umbilical, side view).
Two species from the Kimmeridgian were also selected,
Using a Zeiss Xradia 520 Versa
CT-scan specifications used by specimen. Multiple scans were taken with Xradia as high-quality scans take a long time, so preliminary scans were done first.
Individual slices (tomographs) were viewed by selecting orthoslices in
different planar views. A 3-D model was rendered with the isosurface
function. Height, length, and width, as well as the spire height and opening
rate, were measured and then used to calculate the height
Scanning electron microscopy was used to study the differences in wall
texture between
As expected, the
Raman spectroscopy graphs comparing three measured specimens,
The
A 3-D reconstruction of
SEM images of
Multiple holes can be seen in the outer chambers of the specimen, the
largest of which is located on the spiral side and is 16
Morphometric growth comparisons between Jurassic species
The maximum length of
A 3-D reconstruction of
The proloculus is small in
Morphometric comparison of each species.
Comprised of 10 sinistrally coiled chambers over two whorls,
Measurements on this specimen were challenging as only external analysis was
possible due to the infilling. Tentatively, the proloculus has a size of 25
As with
In this study, we use the full potential of modern analytical techniques to
study the development of early foraminifers. Preservational challenges
hindered part of our analysis of the internal structures. Externally, all
the specimens are well preserved and chamber texture is easily
distinguishable. The poor internal preservation is a result of infilling,
reducing the clarity of various features. Dissolution affects all the
specimens (Fig. 1) but is most pronounced in the Kimmeridgian specimens
The overall morphology of the Jurassic specimens is homologous. All specimens have globular chambers, although individual chamber shape shows some variations. In general, across the analysed taxa, chamber and test size are similar with a consistent bauplan (preset morphology) due to early ontogenetic constraints. All specimens show an exponential growth pattern comparable to modern specimens (Schmidt et al., 2013).
Ontogenetic stages can be categorized broadly by changes in morphology (Brummer et al., 1987; Caromel et al., 2016). In modern foraminifers, there is a difference in allometric rates between the two main groups of globigerinid and globorotaliid species. Globigerinids have easily identifiable growth stages based upon changes in growth rate and qualitative characteristics such as maturation of the wall texture. In contrast, the definitions of the growth stages of the globorotaliids rely more upon changes in chamber shape and are thus more difficult to differentiate. Based on growth rates and developmental transitions, the Jurassic specimens are morphologically closest to the globigerinid group.
Organisms that grow isometrically are normally small and simplistic in
morphology (Stanley, 1973; Gould, 1988). Following this
paradigm, the simple chamber arrangements of Jurassic foraminifers should
suggest isometric growth. While this is true for the juvenile stage in
Despite the overall differences in growth trajectories, all Jurassic
specimens show growth constraints during the juvenile stage. Juvenile
chambers in all studied specimens are so spherical, smooth, and uniform that
they are indistinguishable. Early ontogenetic constraints are also evident
in extant species of both main groups, e.g.
Changes in the timing of development have been linked with change through
evolution (McKinney, 1986), creating variation between specimens.
Although taxonomic links for Jurassic specimens are hard to establish, it
has been suggested that
The surface area of passive feeding organisms provides insight into metabolic efficiency (Signes et al., 1993), while the volume determines overall metabolic requirements. In planktic foraminifers, volume indicates reproductive success as all the cytoplasm will be converted into gametes in the terminal stage. The constraint on chamber form and growth in the juvenile stage results in higher SAV ratios than in adult foraminifers. During the earlier stages of development specimens have a higher SAV (Fig. 6) optimized for rapid food uptake to sustain a potentially high metabolic activity. Allometric growth through ontogeny results in a decline in SAV and thus metabolic efficiency. In modern species, surface area and volume are related to trophic behaviours: juveniles are herbivorous surface dwellers (Hemleben et al., 1989) but develop to become more specialized (Grigoratou et al., 2019). The benefit of herbivory for early developmental stages was also suggested by a trait modelling approach as it provides small specimens with an optimum size prey which is abundant in all environments (Grigoratou et al., 2019). A low metabolic efficiency is suggested by the decline in the SAV ratio through the adult stage, which in modern species has been related to the change to the carnivorous diet (Hemleben et al., 1989; Caromel et al., 2016). In the same model, adult foraminifera needed to be more generalist, especially in oligotrophic environments, to sustain their energetic needs. This might be specifically true during the Jurassic before the development of large phytoplankton such as diatoms (Kooistra et al., 2007).
Experiments have shown that modern planktic foraminifera exhibit strong
morphological plasticity as a result of the environment they inhabit
(Hecht, 1976; Hecht et al., 1976; Malmgren and
Kennett, 1976; Renaud and Schmidt, 2003). The Jurassic species all possess
globular chambers, with some differentiation on the height and length of
each chamber. By analogy to modern species and disparity after crisis
(Cifelli, 1969), the simple globular chambers suggest that
the Jurassic specimens were not specialized. It has been suggested that
there is a typical size ratio between predator and prey of
The adult test size increases between the Bathonian (104 to 127
Jurassic foraminiferal disparity is low as all species have globular chambers with minor differences in shape. The small number of chambers compared to modern species is interpreted as resulting from a short life cycle (compared to modern specimens) and might be the result of rapid reproduction in nutrient-rich coastal environments. Therefore, our findings support the idea that these were opportunistic bloom species.
The comparison of the ontogenetic sequence between species suggests that juveniles are constrained throughout their morphological evolution akin to modern species. The high SAV ratios point towards the need to satisfy a higher metabolic demand compared to the adult specimens.
Disparity of adult planktic foraminifers increases throughout their evolution. Despite this increase, extant planktic foraminifers show the same ontogenetic constraints as their earliest ancestors, suggesting that there is a specific bauplan operating on all planktic foraminifers.
The data can be downloaded at
Any sample requests should be addressed to Felix Gradstein.
DNS and FG designed the project, CJ performed the CT analysis, OTL the Raman spectroscopy, and SK all other analysis. SK and DNS wrote the paper, and all other authors contributed to the interpretation.
The authors declare that they have no conflict of interest.
Daniela N. Schmidt acknowledges funding from the Royal Society via a Wolfson Merit Award and OTL through a University Research Fellowship (no. UF150057); Sophie Kendall received funding from the University of Bristol Alumni Foundation.
This paper was edited by Kirsty Edgar and reviewed by Matías Reolid and one anonymous referee.