Population dynamics and reproduction strategies of planktonic foraminifera in the open ocean

Abstract

Abstract. It has long been assumed that the population dynamics of planktonic foraminifera is characterised by synchronous reproduction associated with ontogenetic vertical migration. However, due to contradictory observations, this concept became controversial, and subsequent studies provided evidence both in favour and against these phenomena. Here we present new observations from replicated vertically resolved profiles of abundance and shell size variation in four species of planktonic foraminifera from the tropical Atlantic to test for the presence, pattern, and extent of synchronised reproduction and ontogenetic vertical migration in this oceanic region. Specimens of Globigerinita glutinata, Globigerinoides ruber ruber, Globorotalia menardii and Orbulina universa were collected over the first 700 m resolved at nine depth intervals at nine stations over a period of 14 d. Dead specimens were systematically observed irrespective of the depth interval, sampling day and size. Conversely, specimens in the smaller size fractions dominated the sampled populations at all times and were recorded at all depths, indicating that reproduction might have occurred continuously and throughout the occupied part of the water column. However, a closer look at the vertical and temporal size distribution of specimens within each species revealed an overrepresentation of large specimens in depths at the beginning of the sampling (shortly after the full moon) and an overrepresentation of small individuals at the surface and subsurface by the end of the sampling (around new moon). These observations imply that a disproportionately large portion of the population followed for each species a canonical reproductive trajectory, which involved synchronised reproduction and ontogenetic vertical migration with the descent of progressively maturing individuals. This concept is consistent with the initial observations from the Red Sea, on which the reproductive dynamics of planktonic foraminifera has been modelled. Our data extend this model to non-spinose and microperforate symbiont-bearing species, but contrary to the extension of the initial observations on other species of foraminifera, we cannot provide evidence for ontogenetic vertical migration with ascent during maturation. We also show that more than half of the population does not follow the canonical trajectory, which helps to reconcile the existing contrasting observations. Our results imply that the flux of empty shells of planktonic foraminifera in the open ocean should be pulsed, with disproportionately large amounts of disproportionately large specimens being delivered in pulses caused by synchronised reproduction. The presence of a large population reproducing outside of the canonical trajectory implies that individual foraminifera in a fossil sample will record in the calcite of their shells a range of habitat trajectories, with the canonical trajectory emerging statistically from a substantial background range.

Reproduction dynamics of planktonic microbial eukaryotes in the open ocean

“…In nature, planktonic Foraminifera generally occur in very low abundances [30,31]. Temporal synchronization of their reproductive cycles was therefore suggested as a requirement to sustain a population, driven by either lunar cyclicity [7][8][9]32,37] or higher order cyclicities [9,57,58]. Our data support the need for temporally synchronized sexual reproduction to avoid unsustainably low numbers of gamete fusions.…”

“…Spatial concentration of adults could further aid reproductive efforts, for instance by sinking to a physical boundary layer like the halocline, which was repeatedly suggested for planktonic Foraminifera [9,58,60,61]. The turbulent nature of the ocean seems to promote the concentration of plankton into spatial clusters for reproductive purposes on smaller scales, although it may lead to segregation of populations on larger scales [31,62,63].…”

“…Purely sexually reproducing planktonic species must have developed efficient strategies to overcome the obstacle of mate encounter to maintain gene flow across areas with low population densities. Such adaptive strategies include the synchronization of reproduction in time or space [7][8][9], mate detection mechanisms through chemical communication [10], the generation of reproductive cysts [11], or the production of eggs [12] or numerous motile gametes [13,14]. The micro-and meso-zooplankton, such as marine planktonic protists, are especially affected by this problem: due to their small size and limited means for active locomotion [15], they are subjected to passive dispersal by ocean currents.…”

“…However, when considering the patchy occurrence of planktonic Foraminifera in the open ocean with very low population densities [30,31], the question arises as to whether viable populations can be maintained by sexual reproduction alone. So far, it remains debated if this can be achieved by random gamete encounters or if further adaptive strategies, like temporal/spatial synchronization of reproduction as suggested for some species [7][8][9]32] or communication via chemical traits, are necessary to enhance gamete encounter rates.…”

Calcification, Dissolution and Test Properties of Modern Planktonic Foraminifera From the Central Atlantic Ocean

“…The ability of non-motile plankton to inhabit specific depths in the water column requires a means of regulating buoyancy and foraminifera may have different strategies (e.g., low-density metabolic products) for short-term displacement or micro-positioning in the water column, such as any diurnal migrations (Hemleben et al, 1989). For longer term regulation of vertical habitat depth, shell density control during biomineralization provides an inert way for non-motile plankton to regulate flotation and increase negative buoyancy (Marszalek, 1982;Campbell and Dower, 2003) as it grows larger during the long term, ontogenic vertical decent (Meilland et al, 2021).…”