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Experimental assessments of species vulnerabilities to ocean acidification are rapidly increasing in number, yet the potential for short- and long-term adaptation to high CO₂ by contemporary marine organisms remains poorly understood. We used a novel experimental approach that combined bi-weekly sampling of a wild, spawning fish population (Atlantic silverside Menidia menidia) with standardized offspring CO₂ exposure experiments and parallel pH monitoring of a coastal ecosystem. We assessed whether offspring produced at different times of the spawning season (April to July) would be similarly susceptible to elevated (~1100 μatm, pHNIST = 7.77) and high CO₂ levels (~2300 μatm, pHNIST = 7.47). Early in the season (April), high CO₂ levels significantly (p < 0.05) reduced fish survival by 54% (2012) and 33% (2013) and reduced 1 to 10 d post-hatch growth by 17% relative to ambient conditions. However, offspring from parents collected later in the season became increasingly CO₂-tolerant until, by mid-May, offspring survival was equally high at all CO₂ levels. This interannually consistent plasticity coincided with the rapid annual pH decline in the species’ spawning habitat (mean pH: 1 April/31 May = 8.05/7.67). It suggests that parents can condition their offspring to seasonally acidifying environments, either via changes in maternal provisioning and/or epigenetic transgenerational plasticity (TGP). TGP to increasing CO₂ has been shown in the laboratory but never before in a wild population. Our novel findings of direct CO₂-related survival reductions in wild fish offspring and seasonally plastic responses imply that realistic assessments of species CO₂-sensitivities must control for parental environments that are seasonally variable in coastal habitats.

Given finite resources, intense investment in one life history trait is expected to reduce investment in others. Although telomere length appears to be strongly tied to age in many taxa, telomere maintenance requires energy. We therefore hypothesize that telomere maintenance may trade off against other life history characters. We used natural variation in laboratory populations of Atlantic silversides (Menidia menidia) to study the relationship between growth, fecundity, life expectancy, and relative telomere length. In keeping with several other studies on fishes, we found no clear dependence of telomere length on age. However, we did find that more fecund fish tended to have both reduced life expectancy and shorter telomeres. This result is consistent with the hypothesis that there is a trade-off between telomere maintenance and reproductive output.

Global oceans are undergoing acidification and deoxygenation, yet the concurrent effects of low oxygen and acidification on marine fish are unknown. This study quantified the separate and combined effects of low pH and low oxygen on 4 vital early life-history traits (time-to-hatch, hatching success, post-hatch survival, and growth) of 3 ecologically important estuarine fish species (Menidia beryllina, Menidia menidia, and Cyprinodon variegatus). Offspring were exposed from the egg through the early larval stages to ideal (pHT [pH total scale] = 7.9, DO [dissolved oxygen] = 9.0 mg l−1), hypoxic (DO = 1.6–2.5 mg l−1), acidified (pHT = 7.4), and hypoxic + acidified (pHT = 7.4, DO = 1.6–2.5 mg l−1) conditions. Hypoxia alone significantly delayed hatching of embryos by 1 to 3 d and reduced hatching success of all 3 species by 24 to 80%. Acidification alone significantly depressed the survival of M. beryllina. Acidification and hypoxia had an additive negative effect on survival of M. beryllina, a seasonal, synergistic negative effect on survival of M. menidia, and no effect on survival of C. variegatus. Acidification and hypoxia had an additive negative effect on length of larval M. beryllina, while hypoxia alone significantly reduced length of M. menidia and C. variegatus from 15 to 45%. Our findings suggest a greater sensitivity of early life estuarine fish to low oxygen compared to low pH conditions, while also demonstrating that the co-occurrence of both stressors can yield both additive and synergistic negative effects on survival and other fitness-related traits. The reduced fitness of forage fish when experiencing acidification and hypoxia may limit the productivity of higher trophic organisms that depend on them as prey.

Hypoxia (low dissolved oxygen [DO]) and CO₂-induced acidification are important aquatic stressors that are exacerbated by anthropogenic nutrient inputs and are expected to increase in severity with increasing atmospheric CO₂ and higher global temperatures. Understanding how species respond to changes in DO and pH is critical to predicting how climate change will affect estuarine ecosystems, including the extreme shallow margins of these systems, where factors such as respiration, photosynthesis, and tides create daily fluctuations of DO and pH, and strong correlations between the 2 stressors. To determine how acidification affects the sensitivity to hypoxia of 2 important forage fishes, the silversides Menidia menidia and M. beryllina, we recorded opercula ventilation rates, aquatic surface respiration (ASR, where fish breathe in the oxygenated surface layer during hypoxic events), and mortality as we lowered either DO or both DO and pH simultaneously. Fish subjected to low DO and low pH in the laboratory performed ASR and died at higher DO concentrations than fish subjected only to hypoxia. Additionally, fish beat their opercula slower, which may have contributed to the differences in ASR and mortality that we saw. These results indicate acidification can increase mortality under hypoxia not only directly but also indirectly by increasing vulnerability to predation during increased use of ASR.

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.

In gonochoristic vertebrates, sex determination mechanisms can be classified as genotypic (GSD) or temperature-dependent (TSD). Some cases of TSD in fish have been questioned, but the prevalent view is that TSD is very common in this group of animals, with three different response patterns to temperature. We analyzed field and laboratory data for the 59 fish species where TSD has been explicitly or implicitly claimed so far. For each species, we compiled data on the presence or absence of sex chromosomes and determined if the sex ratio response was obtained within temperatures that the species experiences in the wild. If so, we studied whether this response was statistically significant. We found evidence that many cases of observed sex ratio shifts in response to temperature reveal thermal alterations of an otherwise predominately GSD mechanism rather than the presence of TSD. We also show that in those fish species that actually have TSD, sex ratio response to increasing temperatures invariably results in highly male-biased sex ratios, and that even small changes of just 1-2 degrees C can significantly alter the sex ratio from 1:1 (males:females) up to 3:1 in both freshwater and marine species. We demonstrate that TSD in fish is far less widespread than currently believed, suggesting that TSD is clearly the exception in fish sex determination. Further, species with TSD exhibit only one general sex ratio response pattern to temperature. However, the viability of some fish populations with TSD can be compromised through alterations in their sex ratios as a response to temperature fluctuations of the magnitude predicted by climate change.

Assessing the potential of marine organisms to adapt genetically to increasing oceanic CO2 levels requires proxies such as heritability of fitness‐related traits under ocean acidification (OA). We applied a quantitative genetic method to derive the first heritability estimate of survival under elevated CO2 conditions in a metazoan. Specifically, we reared offspring, selected from a wild coastal fish population (Atlantic silverside, Menidia menidia), at high CO2 conditions (~2300 μatm) from fertilization to 15 days posthatch, which significantly reduced survival compared to controls. Perished and surviving offspring were quantitatively sampled and genotyped along with their parents, using eight polymorphic microsatellite loci, to reconstruct a parent–offspring pedigree and estimate variance components. Genetically related individuals were phenotypically more similar (i.e., survived similarly long at elevated CO2 conditions) than unrelated individuals, which translated into a significantly nonzero heritability (0.20 ± 0.07). The contribution of maternal effects was surprisingly small (0.05 ± 0.04) and nonsignificant. Survival among replicates was positively correlated with genetic diversity, particularly with observed heterozygosity. We conclude that early life survival of M. menidia under high CO2 levels has a significant additive genetic component that could elicit an evolutionary response to OA, depending on the strength and direction of future selection.

Menidia menidia

Estuarine nekton (fishes, crabs, and shrimps) play key ecological roles and support valuable commercial and recreational fisheries. Long-term research programs focused on nekton can provide insight into community and population-level changes over time, but are uncommon due to funding and logistical constraints. We describe patterns and changes in a nekton assemblage from an intertidal creek in the North Inlet estuary, South Carolina, USA based on 19 years of observations. From 1984 to 2002, biweekly seine collections (approximately every 2 weeks, n = 469) were made in a pool isolated within an intertidal creek at low tide. The assemblage was composed of juvenile and small adult (mostly < 100 mm) fishes, shrimps, and crabs. The 10 most abundant species made up > 97% of the catch; these species included (in descending order): Leiostomus xanthurus, Litopenaeus setiferus, Fundulus heteroclitus, Mugil cephalus, Farfantepenaeus aztecus, Eucinostomus spp., Mugil curema, Fundulus majalis, Menidia menidia, and Brevoortia tyrannus. The assemblage exhibited a distinct seasonality across years, with peak total abundance in mid-spring, peak total biomass in late spring, and highest species richness in late summer and early fall. Total abundance and species richness showed evidence of significant increases across years, total biomass and the Shannon diversity index remained unchanged, and evenness significantly declined. The composition of the assemblage shifted during the sampling period, with the abundance of key year-round residents (F. heteroclitus, M. cephalus) decreasing and warm-season species (L. xanthurus) increasing. Most of the five metrics of the nekton assemblage and the abundances of the five top species were positively correlated with both water temperature and salinity. Direct and indirect effects of hurricanes and storm events on the hydrogeomorphology of the creek and pool were also recognized as influences on the long-term patterns and trends. Long-term (decadal) sampling programs like this can provide important baseline information, and thus insight into the influence of significant weather events and global climate change on nekton populations and their roles in ecosystem dynamics, as well as inform the management of estuaries and fisheries in the southeastern US.

Application of algicides produced by naturally occurring bacteria is considered an environmentally friendly approach to control harmful algal blooms. However, few studies assess the effects of bacterial algicides on non-target species, either independently or with other stressors. Here, we measured sub-lethal effects of dinoflagellate-specific algicide IRI-160AA on the estuarine fish Fundulus heteroclitus and Menidia menidia in laboratory experiments. Plasma cortisol levels were measured to test whether a neuroendocrine stress response was induced in these fish following exposure to the algicide alone, and in combination with diel-cycling hypoxia and/or pH, at 25 and 30 °C. Results show that exposure to IRI-160AA does not significantly affect cortisol levels in either species, at either temperature tested, whether exposure occurs independently or with co-occurring hypoxia and/or pH cycles as potential multiple stressors. These results support the application of IRI-160AA as an environmentally friendly approach to control harmful algal blooms in estuarine environments.