skip to main content

Title: Diel and tidal pCO2 × O2 fluctuations provide physiological refuge to early life stages of a coastal forage fish
Abstract Coastal ecosystems experience substantial natural fluctuations in p CO 2 and dissolved oxygen (DO) conditions on diel, tidal, seasonal and interannual timescales. Rising carbon dioxide emissions and anthropogenic nutrient input are expected to increase these p CO 2 and DO cycles in severity and duration of acidification and hypoxia. How coastal marine organisms respond to natural p CO 2  × DO variability and future climate change remains largely unknown. Here, we assess the impact of static and cycling p CO 2  × DO conditions of various magnitudes and frequencies on early life survival and growth of an important coastal forage fish, Menidia menidia . Static low DO conditions severely decreased embryo survival, larval survival, time to 50% hatch, size at hatch and post-larval growth rates. Static elevated p CO 2 did not affect most response traits, however, a synergistic negative effect did occur on embryo survival under hypoxic conditions (3.0 mg L −1 ). Cycling p CO 2  × DO, however, reduced these negative effects of static conditions on all response traits with the magnitude of fluctuations influencing the extent of this reduction. This indicates that fluctuations in p CO 2 and DO may benefit coastal organisms by providing periodic physiological refuge from stressful more » conditions, which could promote species adaptability to climate change. « less
; ;
Award ID(s):
Publication Date:
Journal Name:
Scientific Reports
Sponsoring Org:
National Science Foundation
More Like this
  1. Concurrent ocean warming and acidification demand experimental approaches that assess biological sensitivities to combined effects of these potential stressors. Here, we summarize five CO2 × temperature experiments on wild Atlantic silverside, Menidia menidia, offspring that were reared under factorial combinations of CO2 (nominal: 400, 2200, 4000, and 6000 µatm) and temperature (17, 20, 24, and 28 °C) to quantify the temperature-dependence of CO2 effects in early life growth and survival. Across experiments and temperature treatments, we found few significant CO2 effects on response traits. Survival effects were limited to a single experiment, where elevated CO2 exposure reduced embryo survival at 17 and 24 °C. Hatch length displayed CO2 × temperature interactions due largely to reduced hatch size at 24 °C in one experiment but increased length at 28 °C in another. We found no overall influence of CO2 on larval growth or survival to 9, 10, 15 and 13–22 days post-hatch, at 28, 24, 20, and 17 °C, respectively. Importantly, exposure to cooler (17 °C) and warmer (28 °C) than optimal rearing temperatures (24 °C) in this species did not appear to increase CO2 sensitivity. Repeated experimentation documented substantial inter- and intra-experiment variability, highlighting the need for experimental replication tomore »more robustly constrain inherently variable responses. Taken together, these results demonstrate that the early life stages of this ecologically important forage fish appear largely tolerate to even extreme levels of CO2 across a broad thermal regime.« less
  2. Despite the remarkable expansion of laboratory studies, robust estimates of single species CO 2 sensitivities remain largely elusive. We conducted a meta-analysis of 20 CO 2 exposure experiments conducted over 6 years on offspring of wild Atlantic silversides ( Menidia menidia ) to robustly constrain CO 2 effects on early life survival and growth. We conclude that early stages of this species are generally tolerant to CO 2 levels of approximately 2000 µatm, likely because they already experience these conditions on diel to seasonal timescales. Still, high CO 2 conditions measurably reduced fitness in this species by significantly decreasing average embryo survival (−9%) and embryo+larval survival (−13%). Survival traits had much larger coefficients of variation (greater than 30%) than larval length or growth (3–11%). CO 2 sensitivities varied seasonally and were highest at the beginning and end of the species' spawning season (April–July), likely due to the combined effects of transgenerational plasticity and maternal provisioning. Our analyses suggest that serial experimentation is a powerful, yet underused tool for robustly estimating small but true CO 2 effects in fish early life stages.
  3. There is increasing recognition that low dissolved oxygen (DO) and low pH conditions co-occur in many coastal and open ocean environments. Within temperate ecosystems, these conditions not only develop seasonally as temperatures rise and metabolic rates accelerate, but can also display strong diurnal variability, especially in shallow systems where photosynthetic rates ameliorate hypoxia and acidification by day. Despite the widespread, global co-occurrence of low pH and low DO and the likelihood that these conditions may negatively impact marine life, very few studies have actually assessed the extent to which the combination of both stressors elicits additive, synergistic or antagonistic effects in marine organisms. We review the evidence from published factorial experiments that used static and/or fluctuating pH and DO levels to examine different traits (e.g. survival, growth, metabolism), life stages and species across a broad taxonomic spectrum. Additive negative effects of combined low pH and low DO appear to be most common; however, synergistic negative effects have also been observed. Neither the occurrence nor the strength of these synergistic impacts is currently predictable, and therefore, the true threat of concurrent acidification and hypoxia to marine food webs and fisheries is still not fully understood. Addressing this knowledge gap will requiremore »an expansion of multi-stressor approaches in experimental and field studies, and the development of a predictive framework. In consideration of marine policy, we note that DO criteria in coastal waters have been developed without consideration of concurrent pH levels. Given the persistence of concurrent low pH–low DO conditions in estuaries and the increased mortality experienced by fish and bivalves under concurrent acidification and hypoxia compared with hypoxia alone, we conclude that such DO criteria may leave coastal fisheries more vulnerable to population reductions than previously anticipated.« less
  4. Abstract

    The eastern oyster, Crassostrea virginica, forms reefs that provide critical services to the surrounding ecosystem. These reefs are at risk from climate change, in part because altered rainfall patterns may amplify local fluctuations in salinity, impacting oyster recruitment, survival, and growth. As in other marine organisms, warming water temperatures might interact with these changes in salinity to synergistically influence oyster physiology. In this study, we used comparative transcriptomics, measurements of physiology, and a field assessment to investigate what phenotypic changes C. virginica uses to cope with combined temperature and salinity stress in the Gulf of Mexico. Oysters from a historically low salinity site (Sister Lake, LA) were exposed to fully crossed temperature (20°C and 30°C) and salinity (25, 15, and 7 PSU) treatments. Using comparative transcriptomics on oyster gill tissue, we identified a greater number of genes that were differentially expressed (DE) in response to low salinity at warmer temperatures. Functional enrichment analysis showed low overlap between genes DE in response to thermal stress compared with hypoosmotic stress and identified enrichment for gene ontologies associated with cell adhesion, transmembrane transport, and microtubule-based process. Experiments also showed that oysters changed their physiology at elevated temperatures and lowered salinity, with significantlymore »increased respiration rates between 20°C and 30°C. However, despite the higher energetic demands, oysters did not increase their feeding rate. To investigate transcriptional differences between populations in situ, we collected gill tissue from three locations and two time points across the Louisiana Gulf coast and used quantitative PCR to measure the expression levels of seven target genes. We found an upregulation of genes that function in osmolyte transport, oxidative stress mediation, apoptosis, and protein synthesis at our low salinity site and sampling time point. In summary, oysters altered their phenotype more in response to low salinity at higher temperatures as evidenced by a higher number of DE genes during laboratory exposure, increased respiration (higher energetic demands), and in situ differential expression by season and location. These synergistic effects of hypoosmotic stress and increased temperature suggest that climate change will exacerbate the negative effects of low salinity exposure on eastern oysters.

    « less
  5. The environment experienced during embryonic development is a rich source of phenotypic variation, as environmental signals have the potential to both inform adaptive plastic responses and disrupt normal developmental programs. Environment-by-embryo interactions are particularly consequential for species with temperature-dependent sex determination, a mode of sex determination common in non-avian reptiles and fish, in which thermal cues during a discrete period of development drive the formation of either an ovary or a testis. Here we examine the impact of thermal variation during incubation in combination with developmental exposure to a common endocrine-disrupting contaminant on fitness-related hatchling traits in the American alligator (Alligator mississippiensis), a species with temperature-dependent sex determination. Using a factorial design, we exposed field-collected eggs to five thermal profiles (three constant temperatures, two fluctuating temperatures) and two environmentally relevant doses of the pesticide metabolite dichlorodiphenyldichloroethylene; and we quantified incubation duration, sex ratios, hatchling morphometric traits, and growth (9–10 days post-hatch). Whereas dichlorodiphenyldichloroethylene exposure did not generally affect hatchling traits, constant and fluctuating temperatures produced diverse phenotypic effects. Thermal fluctuations led to subtle changes in incubation duration and produced shorter hatchlings with smaller heads when compared to the constant temperature control. Warmer, male-promoting incubation temperatures resulted in larger hatchlings withmore »more residual yolk reserves when compared to cooler, female-promoting temperatures. Together, these findings advance our understanding of how complex environmental factors interact with developing organisms to generate phenotypic variation and raise questions regarding the mechanisms connecting variable thermal conditions to responses in hatchling traits and their evolutionary implications for temperature-dependent sex determination.« less