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 conditions, which could promote species adaptability to climate change.  more » « less
Award ID(s):
1536165
NSF-PAR ID:
10249928
Author(s) / Creator(s):
; ;
Date Published:
Journal Name:
Scientific Reports
Volume:
9
Issue:
1
ISSN:
2045-2322
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    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 to 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. 
    more » « less
  2. null (Ed.)
    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. 
    more » « less
  3. Abstract

    Organisms are increasingly likely to be exposed to multiple stressors repeatedly across ontogeny as climate change and other anthropogenic stressors intensify. Early life stages can be particularly sensitive to environmental stress, such that experiences early in life can “carry over” to have long‐term effects on organism fitness. Despite the potential importance of these within‐generation carryover effects, we have little understanding of how they vary across ecological contexts, particularly when organisms are re‐exposed to the same stressors later in life. In coastal marine systems, anthropogenic nutrients and warming water temperatures are reducing average dissolved oxygen (DO) concentrations while also increasing the severity of naturally occurring daily fluctuations in DO. Combined effects of warming and diel‐cycling DO can strongly affect the fitness and survival of coastal organisms, including the eastern oyster (Crassostrea virginica), a critical ecosystem engineer and fishery species. However, whether early life exposure to hypoxia and warming affects oysters' subsequent response to these stressors is unknown. Using a multiphase laboratory experiment, we explored how early life exposure to diel‐cycling hypoxia and warming affected oyster growth when oysters were exposed to these same stressors 8 weeks later. We found strong, interactive effects of early life exposure to diel‐cycling hypoxia and warming on oyster tissue : shell growth, and these effects were context‐dependent, only manifesting when oysters were exposed to these stressors again two months later. This change in energy allocation based on early life stress exposure may have important impacts on oyster fitness. Exposure to hypoxia and warming also influenced oyster tissue and shell growth, but only later in life. Our results show that organisms' responses to current stress can be strongly shaped by their previous stress exposure, and that context‐dependent carryover effects may influence the fitness, production, and restoration of species of management concern, particularly for sessile species such as oysters.

     
    more » « less
  4. null (Ed.)
    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 require 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. 
    more » « less
  5. Abstract

    Insect parasitoids, and the arthropod hosts they consume during development, are important ecological players in almost all environments across the globe. As ectothermic organisms, both parasitoid and host are strongly impacted by environmental temperature. If thermal tolerances differ between host insect and parasitoid, then the outcome of their interaction will be determined by the ambient temperature. As mean temperatures continue to rise and extreme temperatures become more frequent, we must determine the effect of high temperature stress on host–parasitoid systems to predict how they will fare in the face of climate change.

    The majority of studies conducted on host–parasitoid systems focus on either performance under constant temperature or a fixed metric of thermal tolerance (CTmax) for individual organisms. However, performance at constant temperatures is not predictive of performance under ecologically relevant, fluctuating temperatures and measurements of thermal thresholds provide little information regarding the effects of temperature throughout development. We address this by testing the effects of increasing mean temperature in both constant and fluctuating (±10°C) environments throughout development on the performance of the parasitoid waspCotesia congregataand its lepidopteran larval host,Manduca sexta.

    The growth ofM. sextawas influenced by mean temperature, diurnal fluctuations and parasitization status. Caterpillar growth rate increased with increasing mean temperature, but decreased in response to diurnal fluctuations and parasitization byC. congregatawasps.

    Wasp survival decreased with increasing mean temperature and with diurnal fluctuations. The effect of diurnal fluctuations was stronger at higher mean temperatures. Diurnal fluctuations at our highest mean temperature treatment (30 ± 10°C) resulted in complete wasp mortality, and parasitized hosts displayed abnormal physiology, wherein they failed to exhibit wasp emergence, did not enter the prepupal stage, continued to feed and grew up to twofold larger than a normal, unparasitized caterpillar.

    Our results indicate hosts and parasitoids in this system have different thermal tolerances during development; the parasitoid wasp suffered complete mortality at a temperature regime that is mildly stressful for the unparasitized caterpillar host species. Our findings suggestC. congregatawill suffer more severely under increasing temperatures thanM. sexta, with cascading trophic and ecological effects.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less