Received: 4 November 2016? |? Revised: 10 March 2017? |? Accepted: 16 March 2017
DOI: 10.1002/ece3.2969
O R I G I N A L  R E S E A R C H
The effects of elevated temperature and dissolved ?CO2 on a 
marine foundation species
Cori J. Speights1 ?|?Brian R. Silliman2?|?Michael W. McCoy1
1Department of Biology, East Carolina 
University, Greenville, NC, USA Abstract
2Division of Marine Science and Understanding how climate change and other environmental stressors will affect spe-
Conservation, Nicholas School of the cies is a fundamental concern of modern ecology. Indeed, numerous studies have 
Environment, Duke University, Beaufort, NC, 
USA documented how climate stressors affect species distributions and population persis-
tence. However, relatively few studies have investigated how multiple climate stress-
Correspondence
Cori J. Speights, Department of Biology, East ors might affect species. In this study, we investigate the impacts of how two climate 
Carolina University, Greenville, NC, USA. change factors affect an important foundation species. Specifically, we tested how 
Email: cori.speights@gmail.com
ocean acidification from dissolution of CO2 and increased sea surface temperatures Funding information 
Funding was provided by East Carolina affect multiple characteristics of juvenile eastern oysters (Crassostrea virginica). We 
University and the North Carolina Wildlife found strong impacts of each stressor, but no interaction between the two. Simulated 
Federation.
warming to mimic heat stressed summers reduced oyster growth, survival, and filtra-
tion rates. Additionally, we found that CO2- induced acidification reduced strength of 
oyster shells, which could potentially facilitate crab predation. As past studies have 
detected few impacts of these stressors on adult oysters, these results indicate that 
early life stages of calcareous marine organisms may be more susceptible to effects of 
ocean acidification and global warming. Overall, these data show that predicted 
changes in temperature and CO2 can differentially influence direct effects on individ-
ual species, which could have important implications for the nature of their trophic 
interactions.
K E Y W O R D S
acidification, climate change, multiple stressors, oyster, warming
1? |?INTRODUCTION into oceans is expected to simultaneously decrease ocean pH by ap-
proximately ?0.0014 to ?0.0024 per year over this same time period 
Anthropogenic climate change is dramatically impacting natural eco- (Rhein et al., 2013). Such dramatic changes are expected to signifi-
systems (Hoegh- Guldberg & Bruno, 2010; IPCC, 2014, Walther et al., cantly impact biodiversity and the normal functioning of ecosystems 
2002). Increasing greenhouse gas (e.g., CO2) (Raynaud et al., 1993) (Doney et al., 2012), but we still do not fully appreciate which species 
concentrations in the atmosphere and rising surface temperatures are will be impacted and to what extent these impacts will be manifested 
leading to changes in weather patterns and the loss of ice sheets which (Moritz & Agudo, 2013). For example, changes in species phenology, 
are contributing to sea level rise and salinity increases in coastal hab- community composition, and range shifts caused by climate change 
itats (Nicholls & Cazenave, 2010). Global mean surface temperature are altering species distributions and the interaction networks experi-
is expected to increase by 0.3–4.8°C (IPCC, 2014) by the end of the enced by many species (Walther et al., 2002). While numerous studies 
twenty- first century, while dissolution of elevated atmospheric CO2 have examined how the effects of climate drivers such as temperature, 
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, 
provided the original work is properly cited.
© 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
3808 ?|?  www.ecolevol.org  Ecology and Evolution. 2017;7:3808–3814.
SPEIGHTS ET al. ?? ? | ?3809
salinity, and pH affect the autecology of individual species (Crain, temperatures reduce energy reserves and increase mortality of adult 
Kroeker, & Halpern, 2008; Parmesan, 2006), relatively fewer studies oysters, and the combined effects of reduced pH (via increased dis-
have attempted to elucidate how multiple global climate change fac- solution of CO2) and temperature causes reductions in shell hardness 
tors affect both physical and biological interactions (Prugh et al., 2009; (Ivanina et al., 2013; Matoo, Ivanina, Ullstad, Beniash, & Sokolova, 
Rosenblatt & Schmitz, 2014). 2013). In contrast, increased temperature has been shown to have 
A recent meta- analysis of 328 studies manipulating at least one no detectable effects on juvenile eastern oysters (Talmage & Gobler, 
climate change variable revealed that multiple stressors often combine 2011). Elevated concentrations of CO2 can negatively impact oyster 
to cause larger effects than expected relative to single stressor manip- calcification response (Ries, Cohen, & Mccorkle, 2009), with the lar-
ulations (Rosenblatt & Schmitz, 2014). Alternatively, simultaneously val stage being more vulnerable than the juvenile stage (Talmage & 
changes to multiple global change factors could create counteractive Gobler, 2011). One study on the larval stage of oysters found mineral 
effects. For example, a decrease in pH can impact the growth and saturation state conditions to have the largest impact on larval oyster 
strength of individuals with calcium carbonate shells (Ivanina et al., shell formation (Waldbusser et al., 2015). However, juvenile eastern 
2013), but with an accompanying increase in temperature, the solu- oysters have increased mortality rates in addition to reduced shell 
bility of carbonate ions is reduced, therefore the negative effects of growth in low pH environments (Beniash, Ivanina, Lieb, Kurochkin, & 
lowered pH may be ameliorated. Other anthropogenic activities such Sokolova, 2010).
as overharvesting of higher trophic level predators (e.g., Callinectes In this study, we build upon these earlier studies by investigating if 
sapidus and Menippe mercenaria) can increase the abundance of me- elevated CO2 and increased temperature will impact juvenile eastern 
sopredators and indirectly alter trophic and nontrophic interactions oyster (Crassostrea virginica): (1) growth, (2) survival, and (3) filtration 
(Silliman & Bertness, 2002). Combined, shifts in pH, temperature, and rate.
predator abundances are likely to impact the structure and diversity 
of coastal communities, especially those formed around foundation 2? |?METHODS
species (e.g., oysters). We must therefore enhance understanding of 
how abiotic global climate change variables interact to affect founda- 2.1?|?Experimental setup
tion species if we are to better predict and mitigate the longer term 
consequences of global change on the proper functioning of marine This experiment was conducted in a flow- through aquaculture sys-
and coastal ecosystems, which are currently understudied in this con- tem at the Duke Marine Laboratory in Beaufort, North Carolina 
text (Griffen, Belgrad, Cannizzo, Knotts, & Hancock, 2016; Prugh et al., (Figure 1). Unfiltered seawater from Back Sound flowed into 
2009; Rosenblatt & Schmitz, 2014). 18.9 L buckets arranged in the center of eight 1.22 × 0.61 m bins. 
Oysters are autogenic foundation species (Dayton, 1973; Ellison Each bucket was equipped with two to three submersible aquar-
et al., 2005; Jones, Lawton, & Shachak, 1994) that create a structur- ium heaters to maintain desired temperature treatments. Heated 
ally complex reef that facilitates other species by providing resources, water flowed from the buckets into two 5.68 L plastic containers 
refugia, and settlement space for sessile individuals (Gutiérrez, Jones, (34.3 × 21.0 × 12.1 cm) containing juvenile oysters (spat). To simu-
Strayer, & Iribarne, 2003). By serving as a barrier between the coast late ocean acidification, CO2 was diffused into one of the two paired 
and the shoreline in many systems, oyster reefs reduce coastal ero- 5.68 L containers. To maintain pH at the desired level, each tank 
sion (Meyer, Townsend, & Thayer, 1997), provide water filtration, was outfitted with a dual regulator equipped with a solenoid valve 
help reduce eutrophication (Newell, 2004), and function as important (purchased from Green Leaf Aquariums). The solenoid valve (which 
nutrient (Smyth, Geraldi, & Piehler, 2013) and carbon sinks (Granek, allowed gaseous CO2 to flow or not flow) was regulated in real time 
Compton, & Phillips, 2009; Volety, Haynes, Goodman, & Gorman, by a pH probe attached to a digital pH monitor. The probe detected 
2014; Wingard & Lorenz, 2014). Oysters are also a valuable fishery the pH of the water and opened or closed the solenoid valve to 
and serve as nursery habitat for other important fisheries and non- maintain the pH at 7.8 (the 2081–2100 year RCP8.5 prediction for 
fishery species. In North Carolina, oyster harvest is estimated to gen- ocean acidification) (IPCC, 2014). This setup allowed simultaneous 
erate between $12.80 and $32.00 per 10 m2 (Grabowski & Peterson, manipulation of both temperature and pH (via ?CO2) of continu-
2007) Unfortunately, a recent synthesis suggest that in almost 40% ously flowing unfiltered seawater. Surface water temperature from 
of estuaries and bays (of 144 evaluated globally) 99% of the oyster which flow- through water was sourced naturally varied, therefore 
reefs are functionally extinct and thus are not providing ecosystem our temperature treatments maintained water temperatures at 
functions and services (Beck et al., 2011). In North Carolina, for exam- approximately 0, 1, 2, and 3°C above ambient (Table 1). Ambient 
ple, tens of millions of dollars is invested in efforts to recover eastern temperatures varied from 18.5 to 30.0°C over the duration of the 
oyster fisheries (Beck et al., 2011) and their biogenically created hab- experiment (Table 2). pH probes were calibrated monthly (or on an 
itat. However, the long- term sustainability of such efforts may not be as needed basis). Temperature and pH were measured twice a day 
realized if scientists do not understand how multiple climate change using secondary handheld probes to insure the system was function-
stressors impact the health and ecology of oysters specifically. ing properly.
Investigations into the effects of acidification or sea surface In May 2015, 1,000 individual oyster (Crassostrea virginica) spats 
temperatures on eastern oysters show variable results. Elevated were obtained from Millpoint Aquaculture in Sea Level, NC. Individual 
3810? |? ?? SPEIGHTS ET al.
F IGURE  1?Experimental setup. Oysters (Crassostrea virginica) were placed in one of eight possible treatments. There were four temperature 
treatments (0, 1, 2, 3°C above ambient temperature) that heated two containers each, and one of the two containers received an input of CO2 
(Note: Each CO2 treatment had its own CO2 tank) The treatments were each replicated once (top row and bottom row). A total of 60 oysters 
were placed into each container, totaling 120 oysters for each CO2/temperature treatment
TABLE  1?Mean ± SE for temperature and pH of each treatment TABLE  2?Mean ± SE of the ambient temperature and pH for each 
tank month during the experiment (2 June 2015–19 October 2015)
Tank ID Temperature (°C above ambient) pH Month Ambient temperature (°C) Ambient pH
T1A 1.84 ± 0.04 7.80 ± 0.01 June 28.1 ± 0.22 8.05 ± 0.01
T1B 1.86 ± 0.04 8.02 ± 0.01 July 28.1 ± 0.09 8.03 ± 0.01
T2A 0.10 ± 0.02 8.02 ± 0.01 August 27.8 ± 0.1 8.01 ± 0.01
T2B 0.10 ± 0.02 7.83 ± 0.01 September 26.4 ± 0.19 8.07 ± 0.02
T3A 2.88 ± 0.04 8.01 ± 0.01 October 23.1 ± 0.26 7.97 ± 0.02
T3B 2.89 ± 0.04 7.77 ± 0.01 June and October were not complete months.
T4A 1.17 ± 0.03 8.01 ± 0.01
T4B 1.13 ± 0.03 7.78 ± 0.01
T5A 1.05 ± 0.04 7.78 ± 0.01 (total of 60 oysters per container, 120 per treatment) and weighed on 
T5B 1.09 ± 0.04 8.01 ± 0.01 a weekly basis. After 2 months, oyster tanks were supplemented with 
21.5 ml of a 1/10 dilution of Shellfish Diet 1800 (Reed Mariculture, 
T6A 0.24 ± 0.02 7.78 ± 0.01
Inc.). To add the supplemental diet, water flow was briefly stopped 
T6B 0.13 ± 0.02 8.02 ± 0.01
(1 hr each day), and oxygen was bubbled into the tanks to keep ac-
T7A 2.90 ± 0.04 8.01 ± 0.01
ceptable DO (dissolved oxygen) levels. After 5 months, all oysters 
T7B 2.99 ± 0.04 7.84 ± 0.01 were photographed for height (2.01 ± 0.03 cm average) and survival 
T8A 1.97 ± 0.03 7.80 ± 0.01 was quantified.
T8B 2.05 ± 0.03 8.01 ± 0.01
Temperatures are displayed as degrees above ambient temperature. Each 2.2?|?Oyster shell strength experiment
set of heaters managed two tanks (e.g., T1A and T1B), and within those 
two tanks one received additional CO2 (e.g., T1A) lowering the pH. After 5 months, all remaining oysters were sacrificed and stored at 
20°C. Ten individuals from each treatment were randomly chosen 
for a shell strength assay. Before each assay, we measured height 
oysters were pooled into groups of 10 and placed into 24 in. (61 cm) (distance from umbo to dorsal edge) (mm), length (distance between 
mesh mariculture bags. For each group of ten, we quantified initial anterior and posterior margin) (mm), and whole oyster shell thick-
wet weight (g) using an electronic balance (Ohaus Valor 3000) with ness (largest distance between the outsides of the closed vales) (mm) 
a readability of 0.01 g and photographed (Cannon T5, 55 mm lens) with digital calipers. To determine the relative force needed to crush 
each group to measure oyster height (distance from umbo to dorsal each oyster, they were individually placed under a flat metal surface 
edge) using Image J software (1.44 ± 0.02 cm average). Oyster bags beneath the outer edge of an 18.9 L bucket. Sand was added to the 
were then randomly assigned to a specific CO2/temperature treat- bucket at a slow but continuous rate until the oyster shell was crushed 
ment. Six bags of oysters were placed into each experimental arena (Osenberg & Mittelbach, 1989). The mass needed to crush the shell 
SPEIGHTS ET al. ?? ? | ?3811
(kg) was recorded as a relative measure of shell crushing resistance (an 3? |?RESULTS
important deterrent of mud crab predation).
3.1?|?Effects of CO2 and temperature on oysters
2.3?|?Filtration experiment
Oyster height (mm) decreased with increasing temperature over the 
Approximately 3 months into the experiment, five oysters from course of the experiment (df = 1, ?2 = 4.4798, p = .034; Figure 2). 
each CO2/temperature were randomly selected, and wet weights There was no relationship between oyster wet weight and tempera-
(g) were recorded. Each group of five oysters was placed into a ture (df = 1, ?2 = 0.1586, p = .69; Figure 3). However, there was a sig-
50 ml nalgene tube for the assay. A tube with no oysters was used nificant reduction in oyster survivorship (df = 1, ?2 = 9.584, p = .001; 
as a control for this experiment. The tube was filled with 25 ml of Figure 4) with increasing temperature. There was no impact of el-
water from each individual tank and 3 ml of Shellfish Diet 1800 evated CO2 on oyster height (df = 1, ?
2 = 0.0199, p = .88; Figure 2), 
(1/10 dilution). The lids were left off to allow oxygen and then left oyster survival (df = 1, ?2 = 0.4041, p = .52; Figure 4), or wet weight of 
undisturbed for 1.5 hr. After 1.5 hr, the tubes were lightly shaken oysters (df = 1, ?2 = 0.1717, p = .67; Figure 3).
to insure re- oxygenation of the water and resuspension of shell- Oysters grown in elevated CO2 environments also required sig-
fish diet; after 6 hr, 10 ml of tank water was added to the respec- nificantly less crushing force than oysters in ambient CO2 conditions 
tive tube, and after 7.5 hr the tubes were shaken a second time. (df = 1, F = 6.96, p = .01; Figure 5). While whole oyster shell thickness 
To determine the amount of feces produced by oysters, a proxy affected the amount of weight to crush oysters (df = 1, F = 38.688, 
for oyster filtration, the samples from each tube were run through p < .001; Figure 5), there was no relationship between temperature 
vacuum filtration using 47 mm glass microfiber filters. After each and crushing force, or temperature and oyster shell thickness.
sample was filtered, all equipment was rinsed in water followed by Oysters filtered less from the water (as measured by fecal produc-
a 70% ethanol solution. Each sample was run through filtration for tion) as temperature increased (df = 1, ?2 = 3.9089, p = .048; Figure 6). 
five minutes and afterward placed in a 60°C oven for 1 week. Each There was no impact of elevated CO2 on oyster filtration (df = 1, 
filter was weighed on an electronic balance before filtration and ?2 = 0.4902, p = .48, Figure 6).
after drying. This experiment was replicated three times in each of 
two time blocks separated by ~1.5 months.
4? |?DISCUSSION
2.4?|?Statistics In this study, we found that oysters grown in higher temperatures had 
decreased growth (Figure 2) and survival (Figure 4). Moreover, oysters 
All data were analyzed in the R statistical programing environment (R 
Core Team, 2016). For all analyses, we used median temperature from 
daily measurements as a continuous covariate, and CO2 was treated as 
a two level factor: elevated or ambient CO2. To analyze oyster height 
(mm) and wet weight (g), we used linear mixed effects models (LMM), 
where CO2 and temperature were treated as fixed effects, and tank ID 
was treated as a random effect to account for autocorrelated errors 
among individuals reared in the same tank. To analyze oyster survival, 
we used a generalized linear mixed effects model (GLMM) with a bi-
nomial family error distribution. CO2 and temperature were treated as 
fixed effects, and tank ID as a random effect. We also added an indi-
vidual level random effect to account for mild overdispersion in the 
data (Bates, Mächler, Bolker, & Walker, 2015). Relative crush force 
data were analyzed using a linear model (LM). Oyster shell thickness 
was treated as a continuous covariate in the model. Additionally, oys-
ters were pooled by treatment and then randomly selected for ex-
perimentation to insure that any error due to individuals being reared 
in a common environment was randomly redistributed into the over-
all residual error for model fits. Filtration data were analyzed using 
a LMM, where CO2 and temperature were treated as fixed effects, F IGURE  2?Shell height. Temperature is displayed as degrees 
and tank ID and time block (one or two) were treated as random ef- Celsius above ambient, and growth is a measure of the log difference 
fects. Inferences from LMs, GLMs, LMMs, and GLMMs are based on between final and initial oyster height (n = 92). Lines represent 
predicted values of either elevated (black) or ambient (gray) CO . 
likelihood ratio tests comparing models with and without target fixed 2Individual points represent the average growth using the raw data 
effects. Model assumptions were evaluated visually using QQ plots, elevated (?) or ambient (?) CO2 with horizontal and vertical error 
residual plots, and likelihood profiles, as appropriate. bars representing the standard deviations
3812? |? ?? SPEIGHTS ET al.
F IGURE  3?Wet weight. Temperature is displayed as degrees F IGURE  4?Proportion of oysters alive (before the mud crab 
Celsius above ambient, and wet weight is a measure of the log (Panopeus spp.) predator trials). Temperature is displayed as 
difference between final and initial oyster wet weight (n = 92). Lines degrees Celsius above ambient, and survival is the final divided by 
represent predicted values of either elevated (black) or ambient (gray) initial number of oysters alive (n = 96). Lines represent predicted 
CO2. Individual points represent the average growth using the raw values (binomial error distribution) of either elevated (black) or 
data elevated (?) or ambient (?) CO2 with horizontal and vertical ambient (gray) CO2, and the corresponding envelopes represent 
error bars representing the standard deviations 95% confidence intervals. Individual points represent the average 
proportion alive using the raw data for elevated (?) or ambient (?) of 
CO
grown in elevated CO2 environments had weaker shells (Figure 5). By 
2
quantifying the effects of temperature and CO2 on oysters, we un-
covered differential impacts of multiple stressors on these organisms therefore the observed decrease in oyster filtration could be cor-
that would have been undetected when focused solely on a single related with the decrease in oyster shell height (Figure 2).
interaction. Unlike studies such as Sanford et al. (2014) that found Olympia 
The significant decrease in oyster height without changes in shell oysters raised under elevated CO2 conditions were smaller than those 
thickness suggests temperature dependent deposition of carbonate raised under ambient, we found no significant difference between el-
ion placement during shell formation. Indeed, other studies have evated and ambient treatments for oyster shell height. This suggests 
documented no differences in shell height yet increases in shell thick- that increasing temperatures can assist in offsetting the effects of acid-
ness as a function of temperature (Lord & Whitlatch, 2014). We also ification. Oysters also tended to have lower survival in elevated CO2, 
found a significant decline in juvenile oyster survival with increas- which is consistent with previous studies that have shown decreases 
ing temperature. This result contrasts with studies such as Talmage in oyster survival with an increase in carbon dioxide (Talmage & Gobler, 
and Gobler (2011) that found no significant decline in juvenile oys- 2009). Interestingly, while we found no significant impacts of CO2 or 
ter survivorship with an increase in temperature of 4°C. However, temperature on several oyster traits (such as wet weight and fecal pro-
this difference may be driven in part by differences in experimental duction), CO2 and temperature could strongly affect the strength of 
duration (a shorter duration experiment experiences less mortality) trophic interactions with shell crushing predators such as mud crabs.
or differences in resource availability. In this study, there were low Oysters with significantly weaker shells (Figure 5) may increase the 
levels of natural food resources in the flow- through water during the strength of trophic interactions in oyster reef communities. In fact, a 
first 2 months of our study that may have affected later sensitivity to recent study demonstrated that increased acidification reduces native 
increased temperature. Indeed, similar effects and reductions in sur- mud crab consumption on juvenile eastern oysters (Dodd, Grabowski, 
vival with increases in temperature have been documented in other Piehler, Westfield, & Ries, 2015). However, Dodd et al. (2015) only 
studies (e.g., Ivanina et al., 2013). Finally, increasing temperature also manipulated acidification, and it is likely that the increase in the crab’s 
reduced fecal production by oysters. While decreasing temperatures metabolic rate with increased temperature could outweigh reduced 
has been shown to reduce filtration rates of oysters (Walne, 1972), foraging due to elevated CO2. Indeed, crab metabolism and devel-
we manipulated temperatures above ambient during the warmest opmental rates are known to increase with temperature (Costlow, 
summer months, which may have been sufficiently stressful to re- Bookhout, & Monroe, 1962).
duce oyster feeding rates (e.g., proxy for filtration). In addition, fil- Overall, we found decreased growth and survival as well as less 
tration has been shown to increase with shell height (Walne, 1972), production of fecal matter (e.g., less filtration) in oysters grown in 
SPEIGHTS ET al. ?? ? | ?3813
multiple stressors could lead to significantly higher mortality rates of 
this important foundation species.
In concert, these data support the hypothesis that changes in tem-
perature and CO2 predicted from global climate change can influence 
marine communities via direct effects on individual species, which 
could have important implications for the nature of their trophic inter-
actions. Future research should focus on understanding the integrated 
effects of multiple stressors on trophic interactions. Such data will be 
invaluable to ecologist and managers attempting to understand and 
predict the impacts of climate change on important and in some cases 
economically valuable ecosystems.
ACKNOWLEDGMENTS
For providing laboratory space and experimental assistance, we would 
like to thank the members of the Silliman Laboratory at the Duke 
Marine Laboratory and our laboratory assistants Thomas Guryan and 
Erin Tomaras. Additionally, we would like to thank David Kimmel, 
F IGURE  5?Crush weight (proxy for shell strength). Sand plus 
bucket weight is represented as crush weight (kg) (n = 80). Lines April Blakeslee, Krista McCoy, and the McCoy Labs for comments on 
represent predicted values of either elevated (black) or ambient (gray) previous versions of this work.
CO2, and the corresponding envelopes represent 95% confidence 
intervals. Individual points represent the raw data for elevated (?) or 
ambient (?) CO2 CONFLICT OF INTEREST
The authors declare that they have no conflict of interest.
AUTHOR CONTRIBUTIONS
CJS and MWM formulated the question and experimental design. CJS 
performed the experiments. CJS and MWM analyzed the data. CJS, 
BRS, and MWM wrote the manuscript.
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