scholarly journals Reproduction of a marine planktonic protist: Individual success versus population survival

2020 ◽  
Author(s):  
Manuel F. G. Weinkauf ◽  
Michael Siccha ◽  
Agnes K. M. Weiner

AbstractUnderstanding the biology of reproduction is important for retracing key evolutionary processes in organisms, yet gaining detailed insights often poses major challenges. Planktonic Foraminifera are globally distributed marine microbial eukaryotes and important contributors to the global carbon cycle. Their extant biodiversity shows restricted distribution patterns of some species, whereas others are cosmopolitan in the world ocean. Planktonic Foraminifera cannot be bred under laboratory conditions, and thus details of their life cycle remain incomplete. Solely the production of flagellated gametes has been observed and taken as an indication for an exclusively sexual reproduction. Yet, sexual reproduction by spawning of gametes in the open ocean relies on sufficient gamete encounters to maintain viable populations, which represents a problem for organisms that lack the means of active propulsion and are marked by low population densities. To increase knowledge on the reproductive biology of planktonic Foraminifera, we applied a dynamic, individual-based modelling approach with parameters based on laboratory and field observations to test if random gamete encounters under commonly observed population densities are sufficient for maintaining viable populations. We show that temporal synchronization and potentially spatial concentration of gamete release seems inevitable for maintenance of the population. We argue that planktonic Foraminifera optimized their individual reproductive success at the expense of community-wide gene flow, which may explain their high degree of diversity. Our modelling approach helps to illuminate foraminiferal population dynamics and to predict the existence of necessary reproduction strategies, which may be detected in future field experiments. This study therefore contributes to our understanding of plankton ecology and evolution and their reproductive strategies in the open ocean.

2021 ◽  
Author(s):  
Manuel F. G. Weinkauf ◽  
Michael Siccha ◽  
Agnes K. M. Weiner

<p>Understanding the biology of reproduction is important for retracing key evolutionary processes (e.g. speciation and adaptation) in any group of organisms, yet gaining detailed insights often poses a major challenge. Planktonic Foraminifera are a group of globally distributed marine microbial eukaryotes that are important contributors to the global carbon cycle and, due to their fossil record, are widely used as model organisms to investigate the responses of plankton to past environmental changes. The extant biodiversity of planktonic Foraminifera shows restricted distribution patterns and local adaptations of some species, whereas others are cosmopolitan in the world ocean. Hypotheses on their diversification and population dynamics so far entirely rely on the assumption of a nearly exclusively sexual reproduction.</p><p>So far, reproduction in culture has not been successful under laboratory conditions, and thus details on their life cycle and its influence on the evolution of the group remain unknown. Only the production of flagellated gametes has been observed and is taken as an indication for sexual reproduction. Yet, sexual reproduction by spawning of gametes in the open ocean relies on sufficient gamete encounters to maintain viable populations. This represents a problem especially for unflagellated protists like planktonic Foraminifera, which lack the means of active propulsion and are characterized by low population densities in large areas of the world ocean.</p><p>To increase the sparse knowledge on the reproductive biology of planktonic Foraminifera, we applied a dynamic, individual-based modelling approach with parameters based on laboratory and field observations. We tested if random gamete encounters under commonly observed population densities are sufficient for maintaining viable populations or if alternative strategies, such as asexual reproduction or synchronization in depth and time, are indispensable to achieve reproduction success. Our results show that a strict synchronization of gamete release in time and/or space seems inevitable for a successful maintenance of populations. We further argue that planktonic Foraminifera optimized their individual reproductive success at the expense of community-wide gene flow, which may explain their high degree of diversity as well as hampered evolvability. Our modelling approach helps to illuminate the ecology and evolution of this important marine calcifier and to predict the existence of necessary reproduction strategies, which may be detectable in future field and laboratory experiments.</p>


2021 ◽  
Vol 18 (20) ◽  
pp. 5789-5809
Author(s):  
Julie Meilland ◽  
Michael Siccha ◽  
Maike Kaffenberger ◽  
Jelle Bijma ◽  
Michal Kucera

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.


2021 ◽  
Author(s):  
Julie Meilland ◽  
Michael Siccha ◽  
Maike Kaffenberger ◽  
Jelle Bijma ◽  
Michal Kucera

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 favor 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 days. 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 in 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.


1982 ◽  
Vol 17 (2) ◽  
pp. 148-172 ◽  
Author(s):  
Glenn A. Jones ◽  
William F. Ruddiman

AbstractL. V. Worthington (1968, Meteorological Monographs 8, 63–67) hypothesized that a low-salinity lid covered the entire world ocean. By deconvolving isotopic curves from the western equatorial Pacific and equatorial Atlantic, W. H. Berger, R. F. Johnson, and J. S. Killingley (1977), Nature (London) 269, 661–663) and W. H. Berger (1978, Deep-Sea Research 25, 473–480) reconstructed “meltwater spikes” similar to those actually observed in the Gulf of Mexico and thus apparently confirmed the Worthington hypothesis. It is shown that this conclusion is unwarranted. The primary flaw in the reconstructed meltwater spikes is that the mixing intensity used in the deconvolution operation is overestimated. As a result, structure recorded in the mixed isotopic record becomes exaggerated in the attempt to restore the original unmixed record. This structure can be attributed to variable ice-volume decay during deglaciation, effects of differential solution on planktonic foraminifera, temporal changes in abundance of the foraminifera carrying the isotopic signal, and analytical error. An alternative geographic view to the global low-salinity lid is offered: a map showing portions of the ocean potentially affected by increased deglacial meltwater at middle and high latitudes and by increased precipitation-induced runoff at low and middle latitudes.


2020 ◽  
Author(s):  
Holger Pagel ◽  
Björn Kriesche ◽  
Marie Uksa ◽  
Christian Poll ◽  
Ellen Kandeler ◽  
...  

<p>Trait-based models have improved the understanding and prediction of soil organic matter dynamics in terrestrial ecosystems. Microscopic observations and pore scale models are now increasingly used to quantify and elucidate the effects of soil heterogeneity on microbial processes. Combining both approaches provides a promising way to accurately capture spatial microbial-physicochemical interactions and to predict overall system behavior. The present study aims to quantify controls on carbon (C) turnover in soil due to the mm-scale spatial distribution of microbial decomposer communities in soil. A new spatially explicit trait-based model (SpatC) has been developed that captures the combined dynamics of microbes and soil organic matter (SOM) by taking into account microbial life-history traits and SOM accessibility. Samples of spatial distributions of microbes at µm-scale resolution were generated using a spatial statistical model based on Log Gaussian Cox Processes which was originally used to analyze distributions of bacterial cells in soil thin sections. These µm-scale distribution patterns were then aggregated to derive distributions of microorganisms at mm-scale. We performed Monte-Carlo simulations with microbial distributions that differ in mm-scale spatial heterogeneity and functional community composition (oligotrophs, copiotrophs and copiotrophic cheaters). Our modelling approach revealed that the spatial distribution of soil microorganisms triggers spatiotemporal patterns of C utilization and microbial succession. Only strong spatial clustering of decomposer communities induces a diffusion limitation of the substrate supply on the microhabitat scale, which significantly reduces the total decomposition of C compounds and the overall microbial growth. However, decomposer communities act as functionally redundant microbial guilds with only slight changes in C utilization. The combined statistical and process-based modelling approach derives distribution patterns of microorganisms at the mm-scale from microbial biogeography at microhabitat scale (µm) and quantifies the emergent macroscopic (cm) microbial and C dynamics. Thus, it effectively links observable process dynamics to the spatial control by microbial communities. Our study highlights a powerful approach that can provide further insights into the biological control of soil organic matter turnover.</p>


Plant Disease ◽  
2001 ◽  
Vol 85 (5) ◽  
pp. 481-488 ◽  
Author(s):  
F. J. Louws ◽  
M. Wilson ◽  
H. L. Campbell ◽  
D. A. Cuppels ◽  
J. B. Jones ◽  
...  

Acibenzolar-S-methyl (CGA 245704 or Actigard 50WG) is a plant activator that induces systemic acquired resistance (SAR) in many different crops to a number of pathogens. Acibenzolar-S-methyl was evaluated for management of bacterial spot (Xanthomonas axonopodis pv. vesicatoria) and bacterial speck (Pseudomonas syringae pv. tomato) of tomato in 15 and 7 field experiments, respectively. Experiments were conducted over a 4-year period in Florida, Alabama, North Carolina, Ohio, and Ontario using local production systems. Applied at 35 g a.i. ha-1, acibenzolar-S-methyl reduced foliar disease severity in 14 of the 15 bacterial spot and all 7 bacterial speck experiments. Disease control was similar or superior to that obtained using a standard copper bactericide program. Acibenzolar-S-methyl also reduced bacterial fruit spot and speck incidence. Tomato yield was not affected by using the plant activator in the field when complemented with fungicides to manage foliar fungal diseases, but tomato transplant dry weight was negatively impacted. X. axonopodis pv. vesicatoria population densities on greenhouse-grown tomato transplants were reduced by acibenzolar-S-methyl treatment. Bacterial speck and spot population densities on leaves of field-grown plants were not dramatically affected. Acibenzolar-S-methyl can be integrated as a viable alternative to copper-based bactericides for field management of bacterial spot and speck, particularly where copper-resistant populations predominate.


2020 ◽  
Vol 42 (4) ◽  
pp. 403-410 ◽  
Author(s):  
Haruka Takagi ◽  
Atsushi Kurasawa ◽  
Katsunori Kimoto

Abstract Gamete release has been frequently observed in laboratory cultures of various species of planktonic foraminifera. Those observations have been taken as evidence that these organisms produce new generations exclusively by sexual reproduction. We report here the first observation of asexual reproduction in Globigerinita uvula, a small, microperforate foraminifera. The asexual phase was associated with the release of ca. 110 offspring, all of which hosted symbiotic algae that must have been passed on directly from the parent. This event was also the first observation of vertical transmission of symbionts in planktonic foraminifera. Although the trigger of the observed asexual reproduction and its frequency in nature remain unknown, our observation indicates that among the planktonic foraminifera, at least G. uvula has not abandoned the asexual phase of its life cycle.


Sign in / Sign up

Export Citation Format

Share Document