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Biology subjects

Tarrant, A. M.

Publications and source records attributed to Tarrant, A. M..

7 recordsLinked to original sources

Feeding status modulates diel vertical migration ofzooplankton via effects on circadian rhythms

Diel vertical migration (DVM) of aquatic animals is arguably the largest migration on Earth, and occurs each day in most marine and freshwater ecosystems. DVM is influenced directly by factors such as light, food, and predator abundance, but is also regulated by internal circadian clocks. Untangling the mechanistic controls of DVM, and the relative importance of external versus endogenous cues, has been hampered by a lack of experimental systems. Here, we leverage advances in animal tracking software to develop an imaging system allowing us to quantify the positions of dozens of individual copepods (Acartia tonsa) at sub-second resolution over multiple days. We use this approach to characterize group-level diel behavioral patterns at much higher resolution than has previously been possible. We find that behavioral rhythms entrain to light cycles and regular feeding and persist during constant conditions (darkness, no feeding), indicating true circadian regulation and establishing A. tonsa as an experimental system for DVM. We test the hypothesis that food availability impacts DVM by acting as an entraining cue for circadian rhythms. Daytime-restricted feeding weakens circadian behavioral rhythms compared to nighttime-restricted feeding, illustrating that food availability can impact DVM indirectly via effects on internal clocks in zooplankton. Our results provide a detailed view of zooplankton populations over diel cycles, establish a mechanism by which temporal variation in food supply can affect zooplankton migrations, and lay the groundwork for new experimental studies of circadian behavior.

animal behavior and cognition↗

Nutritional condition drives spatial variation in physiology of Antarctic lipid-storing copepods

Lipid-rich copepods form an essential link between primary producers and higher trophic levels in high-latitude oceans. These zooplankton can take advantage of ephemeral phytoplankton blooms to fuel development and reproduction. However, we have limited understanding of how the physiological condition of these animals varies in relation to environmental factors such as food availability. Due to high advection, it is likely that physiological plasticity, rather than local adaptation, is primarily responsible for physiological differences within a region. We use transcriptomics and other physiological metrics to understand how two species of copepods (Calanoides acutus and Calanus propinquus) vary across environmental gradients along the West Antarctic Peninsula. For the primarily herbivorous C. acutus, physiological separation between sampling locations appears to be driven by feeding status, and gene expression differences indicate differential expression of genes regulating lipid metabolism, reproduction, aerobic metabolism, and protein translation. For the more omnivorous C. propinquus, physiology and gene expression did not segregate as clearly by location, showed minimal signs of food deprivation at any location, and had a weaker relationship with chlorophyll compared to C. acutus. By comparing these results with concurrent starvation experiments, we find thatspatial variation in gene expression reflects short-term differences in food availability (particularly for C. acutus,), and we identify genes whose expression indicates recent feeding status. Further examination of the relationships between food availability, copepod physiology, and population dynamics will ultimately improve our capacity to predict how copepod populations will respond to rapidly changing environmental conditions in the West Antarctic Peninsula ecosystem.

ecology↗

Comparative analysis of the molecular starvation response of Southern Ocean copepods

Large lipid-storing copepods dominate mesozooplankton biomass in the polar oceans and form a critical link between primary production and higher trophic levels. The ecological success of these species depends on their ability to survive periods of food deprivation in a highly seasonal environment, but the molecular changes that mediate starvation tolerance in these taxa are unknown. We conducted starvation experiments for two dominant Southern Ocean copepods, Calanoides acutus and Calanus propinquus, allowing us to compare the molecular starvation response between species. These species differ in life history, diet, and metabolic traits, and expressed overlapping but distinct transcriptomic responses to starvation. Most starvation-response genes were species-specific, but we identified a conserved core set of starvation-response genes related to RNA and protein metabolism. We used phylotranscriptomics to place these results in the context of copepod evolution and found that starvation-response genes are under strong purifying selection at the sequence level and stabilizing selection at the expression level, consistent with their role in mediating essential biological functions. Selection on starvation-response genes was especially strong in our focal lipid-storing lineage relative to other copepod taxa, underscoring the significance of starvation tolerance for these species. We also found that certain key lipid enzymes (elongases and desaturases) have experienced diversification and positive selection in lipid-storing lineages, reflecting the unique lipid storage needs of these animals. Our results shed light on the molecular adaptations of high-latitude zooplankton to variable food conditions, and suggest that starvation-response genes are under particularly strong sequence and expression constraints.

evolutionary biology↗

Sea butterflies in a pickle: Reliable biomarkers and seasonal sensitivity of pteropods to ocean acidification in the Gulf of Maine

The passive dissolution of anthropogenically produced CO2 into the ocean system is reducing ocean pH and changing a suite of chemical equilibria, with negative consequences for some marine organisms, in particular those that bear calcium carbonate shells. Although our monitoring of these chemical changes has improved, we have not developed effective tools to translate observations, which are typically of the pH and carbonate saturation state, into ecologically relevant predictions of biological risks. One potential solution is to develop bioindicators: biological variables with a clear relationship to environmental risk factors that can be used for assessment and management. Thecosomatous pteropods, a group of pelagic shelled marine gastropods, whose biological responses to CO2 have been suggested as potential bioindicators of OA owing to their sensitivity to acidification in both laboratory and the natural environment. Using five CO2 exposure experiments, occurring across 4 seasons and running for up to 15 days, we describe a consistent relationship between saturation state, shell transparency, and duration of exposure, as well as identify a suite of genes that could be used for biological monitoring. We clarify variations in thecosome responses due to seasonality, resolving prior uncertainties and demonstrating the range of their phenotypic plasticity. These biomarkers of acidification stress can be implemented into ecosystem models and monitoring programs in regions where pteropods are found, while the approach will serve as an example for other regions on how to bridge the gap between point-based chemical monitoring and biologically relevant assessments of ecosystem health. Summary StatementDespite seasonal variability, pteropods exposed to acidification over multiple seasons reveal consistent patterns in gene expression and shell condition that can be used as bioindicators of ocean acidification stress.

physiology↗

Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis.

Circadian clocks infer time of day by integrating information from cyclic environmental factors called zeitgebers, including light and temperature. Single zeitgebers entrain circadian rhythms, but few studies have addressed how multiple, simultaneous zeitgeber cycles interact to affect clock behavior. Misalignment between zeitgebers ("sensory conflict") can disrupt circadian rhythms, or alternatively clocks may privilege information from one zeitgeber over another. Existing studies are limited in the range of tested zeitgeber relationships, and also in their taxonomic breadth, which is restricted to insects and vertebrates among animals. Here, we show that temperature cycles entrain circadian locomotor rhythms in Nematostella vectensis, a model system for cnidarian circadian biology. We then conduct behavioral experiments across a comprehensive range of light and temperature cycles. Nematostellas circadian behavior is disrupted by chronic sensory conflict, including disruption of the endogenous clock itself rather than a simple masking effect. Sensory conflict also disrupts the rhythmic transcriptome, with numerous genes losing rhythmic expression. However, many metabolic genes remained rhythmic and in-phase with temperature, and other genes even gained rhythmicity, implying that some rhythmic metabolic processes persist even when behavior is disrupted. Our results show that a cnidarian clock relies on information from light and temperature, rather than prioritizing one zeitgeber over the other. Although we identify limits to the clocks ability to integrate conflicting sensory information, there is also a surprising robustness of behavioral and transcriptional rhythmicity.

zoology↗

Plasticity in parental effects confers rapid larval thermal tolerance in Nematostella vectensis

Parental effects can prepare offspring for different environments and facilitate survival across generations. We exposed parental populations of the estuarine anemone, Nematostella vectensis, from Massachusetts to elevated temperatures and quantified larval mortality across a temperature gradient. We find that parental exposure to elevated temperatures results in a consistent increase in larval thermal tolerance (mean ΔLT50: 0.3°C), and larvae from subsequent spawns return to baseline thermal thresholds when parents are returned to normal temperatures. Histological analyses of gametogenesis in females suggests these dynamic shifts in larval thermal tolerance may be facilitated by maternal effects in non-overlapping gametic cohorts. We also compared larvae from North Carolina (a genetically distinct population with higher baseline thermal tolerance) and Massachusetts parents, and found larvae from heat-exposed Massachusetts parents have thermal thresholds comparable to larvae from unexposed North Carolina parents. North Carolina parents also increased larval thermal tolerance under the same high-temperature regime, suggesting plasticity in parental effects is an inherent trait for N. vectensis. Overall, we find larval thermal tolerance in N. vectensis shows both a strong genetic basis and phenotypic plasticity. Further understanding the mechanisms behind these shifts can elucidate the fate of thermally sensitive ectotherms in a rapidly changing thermal environment.Competing Interest StatementThe authors have declared no competing interest.View Full Text

physiology↗

Seasonal variation in physiology and shell condition of the pteropod Limacina retroversa in the Gulf of Maine relative to life cycle and carbonate chemistry.

Natural cycles in the seawater partial pressure of carbon dioxide (CO2) in the Gulf of Maine, which vary from [~]250-550 {micro}atm seasonally, provide an opportunity to observe how the life cycle and phenology of the shelled pteropod Limacina retroversa responds to changing food, temperature and carbonate chemistry conditions. Distributional, hydrographic, and physiological sampling suggest that pteropod populations are located in the upper portion of the water column (0-150 m) with a maximum abundance above 50 m, allowing them to generally avoid aragonite undersaturation. Gene expression and shell condition measurements show, however, that the population already experiences biomineralization stress in the winter months even when aragonite is slightly oversaturated, reinforcing the usefulness of this organism as a bio-indicator for pelagic ecosystem response to ocean acidification. There appear to be two reproductive events per year with one pulse timed to coincide with the spring bloom, the period with highest respiration rate, fluorescence, and pH, and a second more extended pulse in the late summer and fall. During the fall there is evidence of lipid storage for overwintering, allowing the second generation to survive the period of low food and aragonite saturation state. Based on these observations we predict that in the future pteropods will likely be most vulnerable to changing CO2 regionally during the fall reproductive event when CO2 concentration already naturally rises and there is the added stress of generating lipid stores.

ecology↗