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.

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 µm in diameter for the adult specimen) for which the classical approaches of dissecting individual chambers for analysis are ineffective (e.g. Huber, 1994).

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.

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 G. balakhmatovae and G. tojeiraensis, likely in response to the large geochemical gradients indicated by the abundant pyrite in the section (see Sect. 2.1). The tests of earliest Jurassic foraminifers have been documented as aragonitic, but the two Kimmeridgian specimens studied here are calcitic. The most plausible explanation for this is that both G. balakhmatovae and G. tojeiraensis have recrystallized from aragonite to calcite. Aragonite is unstable at low pressures (below ∼0.4 GPa at 300 K) and hence tends to recrystallize when sediments are exhumed (Allison and Bottjer, 2010). This recrystallization (Fig. 5) does not directly affect the evidence of development, but the dissolution within the earliest chambers hinders interpretation. We do not suggest that the “switch” from aragonite to calcite shells occurred prior to the Kimmeridgian.

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 G. bathoniana and G. tojeiraensis, it is not the case in G. oxfordiana or G. balakhmatovae. In these species, shell coiling is planispiral during the juvenile stage. In G. balakhmatovae and G. tojeiraensis, and to a lesser extent in G. bathoniana, growth is not steady throughout development. The early ontogeny of G. tojeiraensis is isometric but by the adult stage is negatively allometric: a feature seen in modern globorotaliid species such as Globorotalia menardii.

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. G. menardii and G. bulloides, indicating that this constraint has been selected for prior to their last common ancestor. G. oxfordiana, G. balakhmatovae, and G. tojeiraensis transition to adult at approximately half their overall size, similar to the modern species G. bulloides and Globigerinella siphonifera. In contrast, G. bathoniana transitions at 80 % of its final size. We speculate that the growth transition is driven by a similar physiological reason necessitating an optimization of surface to volume ratios.

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 G. tojeiraensis is a descendant of G. oxfordiana (Gradstein et al., 2017a). Morphologically, these specimens both show the “standard” simple Jurassic pattern of globular chambers arranged in a low trochospire. However, the developmental path of G. tojeiraensis has a greater resemblance to G. balakhmatovae than to G. oxfordiana. Both G. oxfordiana and G. tojeiraensis grow allometrically during the adult stage. Differentiation of the neanic and juvenile stages of both G. tojeiraensis and G. balakhmatovae proved to be challenging due to the poor preservation and the lack of clear differentiation of features, leading us to separate ontogeny into juvenile and adult stages only. Both G. bathoniana and G. oxfordiana show neoteny, or slow development, indicated by the small increase in size and volume with each new chamber added.

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 10:1 (Kiørboe, 2008), which might explain the small size of Jurassic foraminifers. The final chamber size of both G. balakhmatovae and G. tojeiraensis suggests a growth plateau which might be interpreted as stunted growth due to the lack of optimal environments.

The adult test size increases between the Bathonian (104 to 127 µm) and Kimmeridgian (197 to 246 µm). This observation can be interpreted as an increase in size following Cope's rule or sampling species which are well or less well adapted to the habitat in which we sampled them as stressful habitats have been suggested to lead to smaller size (Schmidt et al., 2004, 2006). Hallam (2001) noted that the size of planktic foraminifers increases during transgressive cycles, which occur through the later Jurassic. These time intervals are overall warm climates with increased shelf habitats; these have been suggested to result in higher diversity and high productivity in the photic zone (Röhl et al., 2001; Gradstein et al., 2017b). Compared to modern species, the Jurassic specimens possess fewer chambers, which may indicate a faster reproduction time. The high population size supported by earlier gametogenesis may indicate an opportunistic species. If true, this hypothesis has two consequences: firstly, it suggests that the population size would have been larger, and secondly it raises the question of whether these specimens had the strong circadian clock which controls reproduction in modern species (Hemleben et al., 1989). The Polish sections contain ammonites, belemnites, bivalves, scaphopods, gastropods, foraminifers, echinoderms, and shark teeth, as well as trace fossils, calcareous nannoplankton, pollen, sphoromorphs, dinoflagellates, and driftwood (Gradstein et al., 2017a), suggesting a shallow-water habitat. If their habitats had been limited to marine continental margin conditions instead of the distal open ocean (Gradstein et al., 2017b) with high population densities, maybe reproduction could have happened more frequently, supported by the higher nutrient availability in these settings.

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.