skip to main content


Title: Naupliar exposure to acute warming does not affect ontogenetic patterns in respiration, body size, or development time in the cosmopolitan copepod Acartia tonsa
Short-term, acute warming events are increasing in frequency across the world’s oceans. For short-lived species like most copepods, these extreme events can occur over both within- and between-generational time scales. Yet, it is unclear whether exposure to acute warming during early life stages of copepods can cause lingering effects on metabolism through development, even after the event has ended. These lingering effects would reduce the amount of energy devoted to growth and affect copepod population dynamics. We exposed nauplii of an ecologically important coastal species, Acartia tonsa , to a 24-hour warming event (control: 18°C; treatment: 28°C), and then tracked individual respiration rate, body length, and stage duration through development. As expected, we observed a decrease in mass-specific respiration rates as individuals developed. However, exposure to acute warming had no effect on the ontogenetic patterns in per-capita or mass-specific respiration rates, body length, or development time. The lack of these carryover effects through ontogeny suggests within-generational resilience to acute warming in this copepod species.  more » « less
Award ID(s):
1947965
NSF-PAR ID:
10412349
Author(s) / Creator(s):
; ;
Editor(s):
Kumar, Ram
Date Published:
Journal Name:
PLOS ONE
Volume:
18
Issue:
4
ISSN:
1932-6203
Page Range / eLocation ID:
e0282380
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Climate change is resulting in increasing ocean temperatures and salinity variability, particularly in estuarine environments. Tolerance of temperature and salinity change interact and thus may impact organismal resilience. Populations can respond to multiple stressors in the short‐term (i.e., plasticity) or over longer timescales (i.e., adaptation). However, little is known about the short‐ or long‐term effects of elevated temperature on the tolerance of acute temperature and salinity changes. Here, we characterized the response of the near‐shore and estuarine copepod,Acartia tonsa, to temperature and salinity stress. Copepods originated from one of two sets of replicated >40 generation‐old temperature‐adapted lines: ambient (AM, 18°C) and ocean warming (OW, 22°C). Copepods from these lines were subjected to one and three generations at the reciprocal temperature. Copepods from all treatments were then assessed for differences in acute temperature and salinity tolerance. Development (one generation), three generations, and >40 generations of warming increased thermal tolerance compared to Ambient conditions, with development in OW resulting in equal thermal tolerance to three and >40 generations of OW. Strikingly, developmental OW and >40 generations of OW had no effect on low salinity tolerance relative to ambient. By contrast, when environmental salinity was reduced first, copepods had lower thermal tolerances. These results highlight the critical role for plasticity in the copepod climate response and suggest that salinity variability may reduce copepod tolerance to subsequent warming.

     
    more » « less
  2. Across diverse taxa, sublethal exposure to abiotic stressors early in life can lead to benefits such as increased stress tolerance upon repeat exposure. This phenomenon, known as hormetic priming, is largely unexplored in early life stages of marine invertebrates, which are increasingly threatened by anthropogenic climate change. To investigate this phenomenon, larvae of the sea anemone and model marine invertebrateNematostella vectensiswere exposed to control (18 °C) or elevated (24 °C, 30 °C, 35 °C, or 39 °C) temperatures for 1 h at 3 days post-fertilization (DPF), followed by return to control temperatures (18 °C). The animals were then assessed for growth, development, metabolic rates, and heat tolerance at 4, 7, and 11 DPF. Priming at intermediately elevated temperatures (24 °C, 30 °C, or 35 °C) augmented growth and development compared to controls or priming at 39 °C. Indeed, priming at 39 °C hampered developmental progression, with around 40% of larvae still in the planula stage at 11 DPF, in contrast to 0% for all other groups. Total protein content, a proxy for biomass, and respiration rates were not significantly affected by priming, suggesting metabolic resilience. Heat tolerance was quantified with acute heat stress exposures, and was significantly higher for animals primed at intermediate temperatures (24 °C, 30 °C, or 35 °C) compared to controls or those primed at 39 °C at all time points. To investigate a possible molecular mechanism for the observed changes in heat tolerance, the expression of heat shock protein 70 (HSP70) was quantified at 11 DPF. Expression of HSP70 significantly increased with increasing priming temperature, with the presence of a doublet band for larvae primed at 39 °C, suggesting persistent negative effects of priming on protein homeostasis. Interestingly, primed larvae in a second cohort cultured to 6 weeks post-fertilization continued to display hormetic growth responses, whereas benefits for heat tolerance were lost; in contrast, negative effects of short-term exposure to extreme heat stress (39 °C) persisted. These results demonstrate that some dose-dependent effects of priming waned over time while others persisted, resulting in heterogeneity in organismal performance across ontogeny following priming. Overall, these findings suggest that heat priming may augment the climate resilience of marine invertebrate early life stagesviathe modulation of key developmental and physiological phenotypes, while also affirming the need to limit further anthropogenic ocean warming.

     
    more » « less
  3. Abstract

    Mortality and shifts in species distributions are among the most obvious consequences of extreme climatic events. However, the sublethal effects of an extreme event can have persistent impacts throughout an individual’s lifetime and into future generations via within‐generation and transgenerational phenotypic plasticity. These changes can either confer resilience or increase susceptibility to subsequent stressful events, with impacts on population, community, and potentially ecosystem processes. Here, we show how a simulated extreme warming event causes persistent changes in the morphology and growth of a foundation species (eelgrass,Zostera marina) across multiple clonal generations and multiple years. The effect of previous parental exposure to warming increased aboveground biomass, shoot length, and aboveground–belowground biomass ratios while also greatly decreasing leaf growth rates. Long‐term increases in aboveground–belowground biomass ratios could indicate an adaptive clonal transgenerational response to warmer climates that reduces the burden of increased respiration in belowground biomass. These transgenerational responses were likely decoupled from clonal parent provisioning as rhizome size of clonal offspring was standardized at planting and rhizome starch reserves were not impacted by warming treatments. Future investigations into potential epigenetic mechanisms underpinning such clonal transgenerational plasticity will be necessary to understand the resilience of asexual foundation species to repeated extreme climatic events.

     
    more » « less
  4. Abstract

    Organisms have the capacity to alter their physiological response to warming through acclimation or adaptation, but the consequence of this metabolic plasticity for energy flow through food webs is currently unknown, and a generalisable framework does not exist for modelling its ecosystem-level effects. Here, using temperature-controlled experiments on stream invertebrates from a natural thermal gradient, we show that the ability of organisms to raise their metabolic rate following chronic exposure to warming decreases with increasing body size. Chronic exposure to higher temperatures also increases the acute thermal sensitivity of whole-organismal metabolic rate, independent of body size. A mathematical model parameterised with these findings shows that metabolic plasticity could account for 60% higher ecosystem energy flux with just +2 °C of warming than a traditional model based on ecological metabolic theory. This could explain why long-term warming amplifies ecosystem respiration rates through time in recent mesocosm experiments, and highlights the need to embed metabolic plasticity in predictive models of global warming impacts on ecosystems.

     
    more » « less
  5. Abstract

    Calanus finmarchicuswere reared from eggs to adults at 12°C and 16°C with non‐limiting food in combination with ambient (600μatm) and high (1100μatm)pCO2. These conditions are likely to be encountered by the species at the southern margins of its biogeographical range by the end of the century. Dry weight (DW), carbon (C) and nitrogen (N) mass, oil‐sac volume (OSV), fatty acid composition (FA), and oxygen consumption rates (OCR) were measured on newly molted stage CV copepodites and recently molted adult females. By focusing our measurements on these precise events in the life cycle, we were able to obtain a more accurate comparison of growth and respiration across treatments. Copepods raised at 12°C had a significantly greater DW, OSV, and C and N mass than those raised at 16°C HighpCO2, independent of temperature, was associated with a further increase in the DW and C content of the copepods. Interactive effects of temperature andpCO2resulted in a larger OSV at low temperature and highpCO2. Mass‐specific respiration rates were significantly lower at lower temperatures and elevatedpCO2suggesting that the increase in mass (DW, C, and OSV) resulted from reduced metabolic cost. The composition of fatty acids in the copepods varied mainly with temperature. Two fatty acids varied withpCO2: 16:0 tended to decrease with higherpCO2and 18:3n−3 tended to increase with higherpCO2. These observations suggest that elevatedpCO2/lower pH in future oceans may have a beneficial effect onC. finmarchicus.

     
    more » « less