ArticlePDF AvailableLiterature Review

Too Hot to Handle: A Meta-Analytical Review of the Thermal Tolerance and Adaptive Capacity of North American Sturgeon

Authors:

Abstract

Understanding how ectotherms may fare with rising global temperatures and more frequent heatwaves is especially concerning for species already considered at‐risk, such as long‐lived, late‐maturing sturgeon. There have been concerted efforts to collect data on the movement behavior and thermal physiology of North American sturgeon to enhance conservation efforts; thus, we sought to synthesize these data to understand how sturgeon respond to thermal stress and what capacity they have to acclimate and adapt to warming. Here, we combined a systematic literature review and meta‐analysis, integrating field‐based observations (distribution and spawning) and laboratory‐based experiments (survival, activity, growth, metabolism, and upper thermal limits) for large‐scale insights to understand the vulnerability of North American sturgeon to rising global temperatures. We summarized the preferred thermal habitat and thermal limits of sturgeon in their natural environment and using meta‐analytical techniques, quantified the effect of prolonged temperature change on sturgeon whole‐animal physiology and acute upper thermal limits. While acclimation did not have significant effects on physiological rates or survival overall, there were positive trends of activity and metabolism in young‐of‐the‐year sturgeons, likely offset by negative trends of survival in early life. Notably, North American sturgeon have a greater capacity for thermal tolerance plasticity than other fishes, increasing upper thermal limits by 0.56°C per 1°C change in acclimation temperature. But with limited laboratory‐based studies, more research is needed to understand if this is a sturgeon trait, or perhaps that of basal fishes in general. Importantly, with these data gaps, the fate of sturgeon remains uncertain as climate change intensifies, and physiological impacts across life stages likely limit ecological success.
1 of 24
Global Change Biology, 2024; 30:e17564
https://doi.org/10.1111/gcb.17564
Global Change Biology
RESEARCH ARTICLE OPEN ACCESS
Too Hot to Handle: A Meta- Analytical Review of the
Thermal Tolerance and Adaptive Capacity of North
American Sturgeon
AngelinaM.Dichiera1 | MadisonL.Earhart2 | WilliamS.Bugg3,4 | ColinJ.Brauner2 | PatriciaM.Schulte2
1Virginia Institute of Marine Science, William and Mary, Gloucester Point, Virginia, USA | 2Department of Zoolog y, The University of British Columbia,
Vancouver, British Columbia, Canada | 3Pacific Salmon Foundation, Vancouver, British Columbia, Canada | 4Department of Forest and Conservation
Sciences, T he University of British Columbia, Vancouver, British Columbia, Canada
Correspondence: Angelina M. Dichiera (dichiera@vims.edu)
Received: 14 June 2024 | Revised: 21 September 2024 | Accepted: 9 October 2024
Funding: This work was supported through a National Science Foundation Postdoctoral Research Fellowship in Biolog y (#2109765) to AMD, a University
of British Columbia Zoology Graduate Fellowship to MLE, and a University of Manitoba Graduate Fellowship to WSB, a Natural Sciences and Engineering
Research Council of Canada (NSERC) Collaborative Research and Development grant (CRDPJ52364 0- 18) to CJB, and a Canada Research Chair (CRC-
2021- 00040), and an NSERC Discovery grant (RGPIN- 2017- 04613) to PMS.
Keywords: acclimation| climate change| conservation| endangered species| phenotypic plasticity| physiology
ABSTRACT
Understanding how ectotherms may fare with rising global temperatures and more frequent heatwaves is especially concerning
for species already considered at- risk, such as long- lived, late- maturing sturgeon. There have been concerted efforts to collect data
on the movement behavior and thermal physiology of North American sturgeon to enhance conservation efforts; thus, we sought
to synthesize these data to understand how sturgeon respond to thermal stress and what capacity they have to acclimate and
adapt to warming. Here, we combined a systematic literature review and meta- analysis, integrating field- based observations (dis-
tribution and spawning) and laboratory- based experiments (survival, activity, growth, metabolism, and upper thermal limits) for
large- scale insights to understand the vulnerability of North American sturgeon to rising global temperatures. We summarized
the preferred thermal habitat and thermal limits of sturgeon in their natural environment and using meta- analytical techniques,
quantified the effect of prolonged temperature change on sturgeon whole- animal physiology and acute upper thermal limits.
While acclimation did not have significant effects on physiological rates or survival overall, there were positive trends of activity
and metabolism in young- of- the- year sturgeons, likely offset by negative trends of survival in early life. Notably, North American
sturgeon have a greater capacity for thermal tolerance plasticity than other fishes, increasing upper thermal limits by 0.56°C per
1°C change in acclimation temperature. But with limited laboratory- based studies, more research is needed to understand if this
is a sturgeon trait, or perhaps that of basal fishes in general. Importantly, with these data gaps, the fate of sturgeon remains uncer-
tain as climate change intensifies, and physiological impacts across life stages likely limit ecological success.
1 | Introduction
Steadily rising global temperatures and the increased fre-
quency of extreme thermal events are reducing suitable hab-
itat for many species, altering ecological interactions, and
at the extreme, potentially causing population collapse and
species extinction (Comte etal.2013; Payne etal.2 016; Perry
etal. 2005; Román- Palacios and Wiens 2020; Stillman 2019;
Sunday, Bates, and Dulvy 2012; Vasseur et al. 2014). Many
fish populations are declining worldwide (Burkhead 2012;
This is a n open access ar ticle under the terms of t he Creative Commons Attr ibution License, which p ermits use, dis tribution and repro duction in any medium, p rovided the orig inal work is
properly cited.
© 2024 T he Author(s). Global Change Biology published b y John Wiley & Sons Lt d.
2 of 24 Global Change Biology, 2024
Dudgeon etal.2006; Moyle and Leidy1992), and their survival
and persistence are, at least in part, dictated by temperature-
dependent physiological processes (Fry 1947; Schulte 2015).
Physiological, behavioral, and evolutionary responses to ther-
mal stress, and the degree to which animals can acclimatize,
are thus thought to underlie which species are “winners” or
“losers” in the face of rising temperatures (Beaman, White,
and Seebacher2016; Morley etal.2019; Seebacher, White, and
Franklin2015; Somero2010).
Recent studies suggest that the upper thermal limits of ec-
totherms may not evolve at a sufficient pace to keep up with
increasing environmental temperatures (Araújo et al. 2013;
Bennett etal.2021; Morgan etal.2020; Sandblom etal.2016),
which is especially concerning for long- lived, late- maturing
species such as sturgeon. Sturgeon are one of the most en-
dangered groups of animals globally (Bemis, Findeis, and
Grande 1997), with all 27 species that comprise the order
Acipenseriformes being classified as vulnerable to critically
endangered (IUCN2022). These long- lived fish have unusually
slow generation times, requiring 15–20 years to reach sexual
maturity (Haxton, Sulak, and Hildebrand2016). This life his-
tory combined with historical overharvesting, current habitat
restrictions, and increasing environmental stressors have con-
tributed to the continued decline of these fishes (Haxton and
Cano 2016). Thus, understanding how sturgeon are impacted
by temperature and the degree to which they may be able to
compensate for negative thermal effects through acclimation is
critically important for predicting their fate in an increasingly
warming world.
While there are certainly limitations to the ecological rele-
vance of acute critical thermal maxima (CTmax) tests (reviewed
by Desforges et al.2023), these measurements allow for broad
insights into thermal tolerance plasticity across taxa. In most
cases, ectotherms have limited capacity for acclimation in their
upper thermal limit (Gunderson and Stillman 2015; Morley
et al. 2019). Ideally, an ectotherm would display perfect com-
pensation for warming by increasing their thermal tolerance
in proportion with the acclimation temperature, where a 1°C
increase in acclimation would correspond to a 1°C increase in
upper thermal limits. Though fish may fare somewhat better
than other taxa, in general, ectotherms do not increase upper
thermal limits more than 0.5°C with 1°C increase in environ-
mental temperature (Gunderson and Stillman2015; Comte and
Olden 2017; Morley et al. 2019; Campos et al. 2021; Ruthsatz
et al. 2024). However, recent studies on sturgeon species in
North America have revealed remarkably high thermal toler-
ance and higher levels of thermal tolerance plasticity than pre-
viously seen for other fish species, with up to 1.2°C increase in
upper thermal limits per 1°C increase in acclimation tempera-
ture (Zhang and Kieffer 2014; Bugg etal.2020, 2023; Earhart,
Blanchard, Strowbridge, etal.2023; Penman etal.2023; Weber,
Dichiera, and Brauner2024).
Having diverged from bony fish 200 million years ago, stur-
geon have remained relatively unchanged morphologically
(Bemis, Findeis, and Grande1997) and genetic ally (Brow nstein
et al. 2024) since the lower Jurassic. Yet Acipenseriformes
have very high levels of ploidy. Where all fish have undergone
at least two whole genome duplication (WGD) events, addi-
tional Acipenseriformes- specific WGDs have given rise to tet-
raploid, octoploid, and dodecaploid species, which have four,
eight, and 12 copies of their genome, respectively (reviewed
by Vasil'ev etal.2010; Schreier etal. 2021). As these genome
duplications are thought to have occurred during periods of
environmental upheaval (Trifonov et al. 2016), polyploidy
may confer greater adaptive potential (Fontana et al. 2004;
Knight, Molinari, and Petrov 2005; Murren etal. 2015; Van
de Peer, Mizrachi, and Marchal2017). Thus, these polyploid
sturgeon may have greater acclimatory capacity due to large
genomes, influencing their ability to plastically respond to
environmental change more so than derived fishes (Havelka
etal. 2011; Trifonov et al.2016; Van de Peer, Mizrachi, and
Marchal2017).
Throughout the last century, there have been concerted ef-
forts to collect data on the movement behavior and thermal
physiology of North American sturgeon to enhance conser-
vation efforts. While there are substantial resources for in-
formation regarding individual sturgeon species and specific
populations (e.g., Hildebrand et al. 2 016; Hilton et al. 2016;
Pollock etal.2015; Rodgers etal.2019), there has been lim-
ited synthesis across species to understand patterns of stur-
geon responses to thermal stress—which can vary across
species and life stage—or their potential for remarkable ther-
mal plasticity. Integrating laboratory- based experiments and
field- based observations is critical for large- scale insights into
population and species trends necessary to inform conserva-
tion and management actions (Cooke etal.2013; Wikelski and
Cooke2006).
Here, we utilized both physiological and ecological data to
understand the vulnerability of North American sturgeon to
rising global temperatures through a quantitative synthesis of
the current literature. The objectives of this study were: (1) to
summarize the preferred thermal habitat and thermal limits of
sturgeon in their natural environment; (2) to quantify the ef-
fect of prolonged temperature change (acclimation) on sturgeon
whole- animal physiology; (3) to characterize their acute upper
thermal limits tested in the lab and their plasticity in thermal
tolerance; and (4) to highlight knowledge gaps for future re-
search. The eight species of North American sturgeon included
in this study inhabit diverse environments from the Atlantic
and Gulf coasts to the Mississippi River and Great Lakes to
the Pacific coast (see Figure 1 for locations of experimental
studies included in this meta- analysis). Some species and pop-
ulations maintain residence in lakes and rivers (e.g., lake stur-
geon; Pollock et al. 2015), while others are highly migratory,
inhabiting riverine, estuarine, and coastal environments at dif-
ferent stages in their life cycle (e.g., Atlantic sturgeon; Hilton
etal.2016). Thus, we hypothesized there may be interspecific
differences in thermal effects and limitations based on habi-
tat or region and intraspecific differences based on life stage.
However, in comparison with other fish species, we predicted
that overall, sturgeon have a greater capacity for thermal ac-
climation based on previous observations of their thermal tol-
erance plasticity. Together, these data provide insight into the
thermal capacity of North American sturgeon and how they
may fare in a warming world.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
3 of 24
2 | Materials and Methods
2.1 | Literature Search and Data Collection
A systematic literature search was conducted according to the
Preferred Reporting Items for Systematic Reviews and Meta-
Analyses (PRISMA) guidelines (Figure2). To identify primary
literature on the therma l effects, optima, a nd limitations of North
American sturgeon species, searches were conducted through
the Clarivate Web of Science and Scopus on 20 September 2023
using the following search terms:
((ALL=(sturgeon)) AND ALL=(thermal* OR
temperature OR warming OR climate OR heat OR
thermoregulat*)) AND ALL=(tolerance OR threshold
OR limit OR resistance OR resilience OR stress* OR
surviv* OR sublethal OR optim* OR maxim* OR
behavior OR recovery OR exercise OR distribution OR
migrat*)
The search resulted in a total of 1578 results. After removing
duplicates between the two searches, 1095 articles were ini-
tially screened for relevance and inclusion based on titles and
abstract information. Studies were excluded if: (1) they were
conducted on species other than North American sturgeon
or (2) they reported genetic, cellular, biochemical, or tissue
response data but did not incorporate another physiological
measurement of thermal effects, optima, or limitations. No re-
views or meta- analyses were included with the exception of one
quantitative review (Baril et al.2018). Baril etal. (2018) used
both published data and personal communications to provide
mean water temperature during lake sturgeon spawning for
three watersheds, and we deemed the personal communica-
tions to be of value here (refer to Table1 of Baril etal.2018 for
details of the personal communications).
After the initial screening, 225 studies were further examined
by assessing the methods, results, and discussion for relevant
data. An additional 48 papers were added from a cited refer-
ence search conducted by searching the reference lists of the
225 studies and subsequently evaluating them for inclusion as
described above. These papers consisted mainly of gray litera-
ture (e.g., technical reports) and theses that were not present in
the Clarivate Web of Science and Scopus searches. Of these 273
studies, 11 studies could not be accessed. All 11 were gray lit-
erature or theses from the cited reference search and were not
available online or in print.
Two hundred and sixty- two studies were then assessed for eli-
gibility and categorized as either observational or experimental
in nature. As such, definitions of thermal optima and limita-
tions differed for each. Experimental studies were evaluated for
inclusion if they measured: (1) temperature effects on activity
(swimming, movement), growth, metabolism, and survival;
(2) upper thermal limits (maximum temperature where loss
FIGUR E  | A map of North America with approximate sturgeon locations from the experimental studies used in this review. Only studies that
provided data for effect size and acclimation response ratio calculations were included in the figure, and as such, they do not encompass the entire
range of each species. River locations are approximate, and for studies where only a hatchery or research facility was listed, those approximate
locations were used. Dot size corresponds to the number of studies in that region/river. The Color of the dot corresponds to species. The color on the
map highlights the latitudinal temperature gradient across North America.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
4 of 24 Global Change Biology, 2024
of equilibrium or death occurs); or (3) thermal preference or
avoidance (when given the choice of different temperatures).
Observational studies were evaluated for inclusion if they mea-
sured: (1) temperature- driven changes, upper limits or optima
for spawning; or (2) upper temperature limits to distribution
(habitat use, migrations, and movements).
Furthermore, experimental studies were assessed for their
appropriate use in effect size calculations (detailed below),
and only studies that reported means, variance, sample sizes,
and acclimation temperatures were retained. Studies with
confounding variables (e.g., salinity > 0 ppt, fluctuating tem-
perature treatments, etc.) were excluded. In total, 97 studies
were excluded where they did not present observational or ex-
perimental thermal effects, optima, or limitations as defined.
A final total of 165 studies were included in this systematic re-
view (see Data Sources in the appendix). Among these studies,
112 studies reported observational data (including review by
Baril et al.2018), and 54 studies reported experimental data.
One study (Chapman and Carr 1995) reported both observa-
tional and experimental data and was recorded separately for
both categories.
FIGUR E  | Preferred Reporting Items for Systematic Reviews and Meta- Analyses (PR ISMA) diagram illustrating the number of publications
found and retained through each stage of the literature review process. Records were initially screened for relevance if they included thermal
effects, optima, or limit data on North American sturgeon species. Relevant records were assessed for eligibility and included if they described
observed temperature- driven changes, limits or optima for spaw ning and distribution (habitat use, migrations, and movements), or experimental
effects of temperature on activity (swimming, movement), metabolism, growth, survival, or thermal limits that met the requirements for effect size
calculations. Thermal limits data are categorized into t wo groups: Upper thermal limits (acutely tested critical thermal maxima, CTmax) and thermal
tolerance plasticity (the capacity to change CTmax with thermal acclimation).
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
5 of 24
This information was used to summarize the total number of
publications reporting thermal effects, optima, or limitations of
North American sturgeon species (Figure3). Twelve of the final
165 publications included data on two species of sturgeon, and
thus for Figures 3 and 4a,b, by including this within- study du-
plication for multiple species, the total number of publications
totals 177 studies. In addition, these studies often reported mul-
tiple metrics of thermal effects, optima, or limitations, or data
regarding multiple life stages. From 165 studies, these categori-
zations resulted in 474 unique reports.
A summar y of the number and proportion of report s (of 474 total)
describing thermal effects, limits, or optima on North American
sturgeon by species, metric, and life stage can be found in
Figure 4. Observational studies accounted for 194 unique re-
ports regarding qualitative data on spawning (includes presence
of spawning adults, eggs, or larvae) or distribution (includes
presence/absence, abundance, habitat use, migrations, and
movements). Experimental studies accounted for 280 unique
reports regarding activity (includes swimming, movement),
growth (includes length or mass change), metabolism (includes
routine, standard, maximum metabolic rates, and absolute aer-
obic scope), survival (includes mortality, hatch success), and
thermal limits (critical thermal maxima). Preference/avoidance
reports were excluded due to the limited number of reports on
experimentally determined thermal preference (6 reports from 4
studies). Studies were categorized by life stage in Figure4b: early
life stage (includes pre- hatch embryos, yolk- sac larvae, exoge-
nously feeding larvae), young- of- the- year (a g e - 0), juvenile (a g e - 1
to maturation, including subadult), adult (spawning- capable), or
not reported (where information was not available). Studies were
further categorized by metric according to life stage (Figure4c)
and species (Figure4d). Activity, growth, metabolism, and sur-
vival data were used to calculate effect sizes. Upper thermal
limits were recorded as reports, and where available, these data
were used to calculate acclimation response ratios as a measure
of thermal tolerance plasticity. For all data, when available, we
also collected additional information regarding: the population
or region the fish originated from, body mass, body length, age,
rearing and acclimation temperatures, rearing and acclimation
duration (in time), interacting stressors, and methods used for
each measurement.
2.2 | Effect Size Calculations
To investigate the effect of prolonged temperature exposure on
sturgeon whole- animal physiology, studies that provided data on
activity, growth, metabolism, or survival were included for effect
size calculations if the study included at least two acclimation tem-
peratures and reported means, variance (standard deviations or
standard errors), and sample sizes in the text, tables, or figures.
Studies that collected data when fish were returned to common
garden conditions were not included in effect size calculations.
Where multiple families, populations, or time points were re-
ported in a single study, these data were included as separate re-
ports. Where growth was reported using multiple metrics (e.g.,
length and mass), length was chosen for effect size calculations to
reduce duplication. Where “total growth” is reported, this refers
to the change in total length (mm) from hatch to timing of emer-
gence (Dammerman, Steibel, and Scribner2016). When available,
means, variance, and sa mple sizes were directly extracte d from the
tables and text provided in the articles and associated supplemen-
tal information. Otherwise, data from figures were digitized using
the metaDigitise package in R (Pick, Nakagawa, and Noble2019).
Data extractions were performed by AMD, MLE, and WSB.
Because responses were measured at different acclimation tem-
peratures, we chose to use a temperature- corrected effect size
calculation for activity, growth, and metabolism to account for
nuisance heterogeneity (Noble etal.2022). Effect sizes were cal-
culated as the log- response ratio corrected by the temperature
coefficient Q10 (lnRRQ10):
where R2 and R1 are the mean responses for the treatment and
control groups, respectively, and T2 and T1 are the temperatures
at which these groups were acclimated. As Q10 is a measure of
the factorial change in a biological rate over a 10°C increase in
temperature, lnRRQ10 accounts for passive plasticity predicted
to occur with changing temperature. Effect sizes were standard-
ized to the control treatment, which included control acclimation
temperature (either stated as “control” in text or inferred from
the temperature prior to acclimation), preferred bottom habitat
lnRR
Q10 =ln
(R
2
R
1)(
10
C
T
2
T
1)
FIGUR E  | Available publications on thermal effects, optima, and limits across North American sturgeon species, published from 1920 to 2024.
Histograms illustrate (a) the number of published articles sorted by decade and (b) in total for each of the eight species of North A merican sturgeon.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
6 of 24 Global Change Biology, 2024
(substrate, if provided), feed ration (1% body mass), and dissolved
oxygen levels where possible (100%). Where more than two accli-
mation temperatures were reported, we chose to standardize to
the control treatment rather than a stepwise comparison to avoid
the minimization or inflation of effect sizes. The sampling vari-
ance of lnRRQ10 was calculated as per Noble etal.(2022):
where SD and N are the standard deviation and sample size of
the treatment and control groups. lnRR (without temperature
correction) and the associated sampling variance were also cal-
culated as a proof- of- principle comparison.
To investigate the effect of temperature on survival (reported as
either a ratio of percent survival or percent mortality), the log
odds ratio (lnOR) was calculated to determine the likelihood
of survival in the treatment group compared with the control
group as per Raynal etal.(2022):
where the proportion of alive fish to dead fish was calculated
based on survival/mortality percent and reported sample size,
and where T2 and T1 are the temperatures at which these groups
were acclimated. For sur vival studies, we chose to exclude reports
of time to mortality in the effect size calculations as these values
were not directly comparable to percent survival or mortality (the
most common method of reporting sur vival data). The sampling
variance of lnOR was calculated as per Raynal etal.(2022):
Data extractions were performed by AMD, MLE, and WSB.
To quantify the thermal tolerance plasticity of North American
sturgeon species, studies that provided data regarding the effects
s
2
lnRRQ10 =
SD
2
2
R2
2
N
2
+SD
2
1
R2
1
N
1
+
10C
T2T1
2
lnOR
=ln
(
AliveT2DeadT2
AliveT1DeadT1
)
s
2
lnOR =
(
1
AliveT2
)
+
(
1
DeadT2
)
+
(
1
AliveT1
)
+
(
1
DeadT1
)
FIGUR E  | Available publications on thermal effects, optima, and limits for North A merican sturgeon species published from 1920 to 202 4 and
the qualitative and quantitative reports extracted from these studies. Histograms illustrate (a) the number of published articles sorted by study type
(experimental or observational) included in this study. Most published articles had several reports of usable data, analyzing multiple life stages,
species, or study metrics within a single published article. (b) represents the percentage of reports that have been conducted at different life stages
for each of the eight species. (c, d) depict the number of reports and the percentage of reports, respectively, of different study metrics (activity,
distribution, growth, metabolism, spawning, survival, and thermal limits) at each life stage across all eight species.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
7 of 24
of thermal acclimation on critical thermal maxima (CTmax) were
used to calculate an effect size specific to thermal tolerance: ac-
climation response ratio (ARR; Claussen 1977). ARRs provide
a quantitative means to compare the change in CTmax across a
variety of acclimation temperatures, indicating the thermal plas-
ticity of an organism. ARR was calculated as follows:
where CTmax2 and CTmax1 are the mean responses for the treat-
ment and control groups, respectively, and
T2
and
T1
are the
treatment and control acclimation temperatures, respectively.
The sampling variance of ARR was calculated as per Pottier
etal.(2022):
where SD and N are the standard deviation and sample size
of the treatment and control groups. Data extractions were
primarily performed by WSB and supplemented by AMD and
MLE.
2.3 | Statistical Analyses
All statistical analyses were performed using RStudio (version
2023.12.1; http:// www. R- proje ct. org/ ). To best interpret the
effects of temperature on North American sturgeon species
(using lnRRQ10 , lnOR, and ARR effect size data) and to con-
trol for nuisance heterogeneity (Noble etal. 2022), multi- level
meta- analytical models were performed using the metafor pack-
age (Viechtbauer2 010; version 4.4- 0) using residual maximum
likelihood (REML). Because multiple effect sizes were reported
from the same studies, study ID was included as an observation-
level random effect in all models. Phylogenetic relatedness was
also included as an observational- level random effect, using
methods according to Pottier et al. (2022). To determine the
effects of temperature on activity, metabolism, growth, sur-
vival, and thermal tolerance plasticity, we estimated the overall
meta- analytical mean, as well as the variation between metrics
reported for each. Statistical significance was assumed if 95%
confidence intervals did not overlap with zero. In addition, we
estimated the percent of variance between effect sizes not ex-
plained by sampling error as I2.
To determine what may explain remaining heterogeneity, we
used meta- regressions to explore the effect of six continuous
moderators: acclimation duration (days), control body mass
(g), experimental body mass (g), control temperature, experi-
mental temperature, and temperature difference between con-
trol and experimental treatments. Full models were assessed as
described above, using the metafor package (Viechtbauer2 010;
version 4.4- 0) and the same random effects. If all six continu-
ous moderators were not reported for an effect size, the effect
size was removed to run the full model without missing values.
We removed effect sizes from the datasets for activity (k = 2),
growth (k = 60), and metabolism (k = 15). Because so few stud-
ies reported body mass and acclimation duration for survival
effect sizes, only control temperature, experimental tempera-
ture, and temperature difference were tested as moderators.
A table of Akaike's information criterion (AIC) was created
using the MuMIn package (https:// CRAN. R- proje ct. org/ packa
ge= MuMIn ), and moderators from the top AIC model were re-
tained in the final model. The effect of each retained moderator
in the final model was estimated in a meta- regression using
the REML method to assess how these moderators contributed
individually as sources of variation for activity, metabolism,
growth, survival, thermal tolerance, and thermal plasticity. All
meta- analytical models were plotted using the orchaRd pack-
age (Nakagawa etal.2023; version 2.0).
To provide additional information on the vulnerability of stur-
geon to warming, we extracted data from the studies herein
regarding baseline CTma x and warm- acclimated CTma x and cal-
culated respective thermal safety margins (TSMs). We calcu-
lated TSM as the difference between CTma x and the respective
environmental (i.e., acclimation) temperature. We then explored
the relationships between sturgeon thermal tolerance plasticity
(ARR), upper thermal limits (CTmax), and vulnerability to
warming (TSM) using regression analyses.
3 | Results
Publications regarding the thermal effects, optima, and lim-
itations of North American sturgeon have increased over the
last century, approximately doubling in number every decade
from the 1980s through the last decade (Figure 3a). Lake
sturgeon (A. fulvescens) is the most studied species of North
American sturgeon (Figure 3b), followed by white sturgeon
(A. transmontanus). The least studied species of sturgeon are
the pallid sturgeon (Scaphirhynchus albus), shovelnose stur-
geon (S. platorynchus), and the Gulf of Mexico sturgeon (A.
oxyrhynchus desotoi), a subspecies of the Atlantic sturgeon
(A. oxyrhynchus). As a note, only eight of the nine species of
North American sturgeon were included in this study, as no
studies on Alabama sturgeon (S. suttkusi) met the inclusion
criteria. In fact, the single study of the 1,095 articles origi-
nally screened that mentioned Alabama sturgeon was a liter-
ature review; however, within this review, no experimental
or observational studies were available for Alabama sturgeon
(Flinders and Wiegand 2014). Earlier publications were fo-
cused on observational studies of temperature effects, optima,
and limits, but the proportion of experimental studies has in-
creased the last decade (Figure4a). The proportion of each life
stage studied per sturgeon species was distinct (Figure 4b).
Strikingly, studies on the thermal effects, optima, and limita-
tions of Gulf of Mexico sturgeon are comprised mainly of stud-
ies on adults and on their distribution. Adult sturgeon were
the most studied of all life stages, specifically regarding the ef-
fects of temperature on spawning and distribution (Figure4c).
The young- of- the- year followed adults in the next most stud-
ied life stage, and much more has been studied on their activ-
ity, growth, metabolism, and thermal limits. Studies on early
life stages focused on survival and growth. The least studied
life stage were juveniles (age 1 to maturation, including sub-
adults). In addition, the proportion of each metric studied per
life stage and per species was distinct (Figure4c,d).
ARR
=
(CT
max2
CT
max1
T
2
T
1)
s
2
ARR =
SD
2
T1
NT1
+SD
2
T2
NT2
1
T2T1
2
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
8 of 24 Global Change Biology, 2024
3.1 | Preferred Temperatures and Thermal Limits
of Sturgeon in the Field
Qualitative data on the thermal optima and limitations for dis-
tribution and spawning varied by species, life stage, and met-
ric (TableS1). For all species, spawning temperatures of adults
were most frequently reported, followed by temperatures that
prompt migration (typically associated with spawning behav-
ior). Almost none of the life stages of Atlantic sturgeon are
found at temperatures greater than 28°C. Peak occurrence in
the Mid Atlantic is found at 18°C (Breece etal.2018), although
Atlantic sturgeon are found across a wide range of tempera-
tures throughout their range. Adults spawn from 14°C, their
lower limit in the St. Lawrence River, Quebec (Caron, Hatin,
and Fortin2002), to ~24°C in the York River, Virginia (Hager,
Watterson, and Kahn2020). Shortnose sturgeon, which inhabits
a similar geographic range to Atlantic sturgeon, spawns any-
where between 9°C and 19°C. However, spawning throughout
their habitat typically occurs within narrow thermal windows,
for example, 10°C–15°C in Saint John River, New Brunswick
(Dadswell 1979) to ~12°C–17°C in Altamaha River, Georgia
(Ingram and Peterson2018).
On the west coast of North America, white sturgeon are found
at cooler temperatures, but this varies depending on the river
system. The lowest reported limit for spawning is ~7°C in the
Kootenai River, Idaho (Paragamian and Wakkinen 2011), and
the warmest occurrence of spawning is 22°C in the San Joaquin
River, California (Jackson, Gruber, and Van Eenennaam2016).
Similarly, green sturgeon occupy and spawn across a wide range
of temperatures. In the Klamath and Rogue Rivers in California
and Oregon, adults are found in highest abundance at 19°C
and are rarely found at temperatures > 24°C or < 5°C (Mora
et al. 2009). However, adult green sturgeon in Willapa Bay,
Washington, are not found at temperatures below 10°C (Moser
and Lindley 2007). Spawning occurs at different temperatures
throughout their range, from 10°C to 18°C in the Rogue River
(Erickson and Webb2007), Oregon, to ~13°C and 14°C in the
Sacramento River, California (Brown2007; Poytress etal.2015).
In the south, adult Gulf of Mexico sturgeon are found between
14°C and 26°C in the Suwan nee River, Florida (Carr, Tatman, and
Chapman1996) and seem to prefer temperatures between 17°C
and 23°C for movement and spawning. Fewer studies have doc-
umented Gulf of Mexico sturgeon spawning compared to other
species, and thus far only in the Suwanee and Choctawhatchee
Rivers, Florida. For pallid sturgeon, 20°C is reported as the
upper limit for spawning and abundance. Spawning generally
occurs between 16°C and 20°C in the Missouri and Yellowstone
Rivers (Fuller, Jaeger, and Webb2008; Kappenman, Webb, and
Greenwood 2013; Elliott et al. 2020), and the highest relative
abundance of young- of- the- year is found at 17°C–20°C in the
middle Mississippi River (Phelps et al. 2010). Shovelnose, on
the other hand, have been found at temperatures ranging from
~9°C to 29°C in similar habitats, and spawning is reported to
occur from 11°C to 23°C throughout their range. However, no
gravid females have been caught when temperatures reach 24°C
in Wabash River, Indiana (Kennedy, Sutton, and Fisher2006),
and in general throughout the lower and middle Mississippi
River, juveniles and adults were not present at temperatures
above 20°C.
3.2 | Effects of Prolonged Temperature Change on
Sturgeon Whole- Animal Physiology
When sturgeon were a cclimated to a change in temperatu re, there
were no significant effects on physiological rates. There was a
weak overall effect on growth (lnRRQ10 = 0.1414; CI = 0.3546,
0.0718; p = 0.1936), and marginal but still insignificant effects on
activit y (lnRRQ10 = 0 .4473; CI = 0.0247, 0.9192; p = 0.0 633) a nd
metabolism (lnRRQ10 = 0.5483; CI = 0.0637, 1.1604; p = 0.0791),
with confidence intervals overlapping zero (TableS2; Figure5).
Overall heterogeneity of these data was high (> 95%). Though
there was no significant overall effect, it should be noted that
the directionality for each physiological trait varied. Simply put,
where lnRRQ10 is zero, this indicates the response of the treat-
ment group is the same as the response of the control group
when differences in temperature between studies are accounted
for and standardized to a 10°C increase in temperature. Where
lnRRQ10 is negative or positive, this indicates the response of the
treatment group is respectively reduced or increased compared
to the control group. Activity and metabolism had a general pos-
itive trend with thermal acclimation, and when examining the
variation within each trait by metric, we found that movement
(lnRRQ10 = 0.6895; CI = 0.2446, 1.1343) and standard metabolic
rate (lnRRQ10 = 1.1148; CI = 0.3634 , 1.86 62) were sign ificantly
positively affected by thermal acclimation (Tables S3 and S4;
Figure5a,b,e,f). In contrast, growth had a general negative trend
with thermal acclimation but no significant effects of thermal
acclimation (Table S5; Figure 5c,d). Survival also had a gen-
eral negative, but insignificant, trend with thermal acclimation
(Figure 6; lnRRQ10 = 0. 4321; CI = 1.0851, 0.2208; p = 0 .194 6);
however, heterogeneity was very low (4.34%).
Though prolonged temperature did not significantly affect ac-
tivity, growth, metabolism, or survival, we assessed potential
moderators of these effects (TableS2). We found that acclimation
duration and experimental body mass were important predictors
for activity and growth. Longer acclimations at warm tempera-
tures increased activity and decreased growth, whereas larger
body mass at warm temperatures decreased activity and in-
creased growth. In addition, warmer experimental temperatures
decreased the growth of sturgeons as well. Finally, body mass
of control treatment fish was an important predictor of metab-
olism, where larger body mass at natural temperatures reduced
metabolism. However, all of these significant predictors had
weak effects (Table S2). Control temperature and temperature
difference were not important predictors for any physiological
rate, nor were there significant moderators for survival.
3.3 | Acute Upper Thermal Limits and Thermal
Tolerance Plasticity of Sturgeon
Because ramp rate has been shown to affect CTmax measure-
ments (Desforges et al. 2023), and for at least one sturgeon
species (Penman et al.2023), prior to pooling data, the rela-
tionship bet ween CTmax and ramp rate was assessed. However,
there was no significant relationship (FigureS1; p = 0.838 , ad-
justed R2 = 0.03, slope = 2.15). Thus, CTmax reported for nat-
ural (i.e., “control”) conditions were pooled across life stages
(dominated by young- of- the- year life stage, ~78% of data)
and ramp rate and analyzed for between- species differences.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
9 of 24
The overall meta- analytical mean CTmax was 30.26°C
(CI = 28.9263, 31.5910; Table S2; Figure 7a), and there were
no statistically significant differences between species' CTmax,
which ranged from ~29.5°C to 32.5°C (TableS6; Figure7c). In
the data set, the highest CTmax value was recorded from YOY
shortnose sturgeon (35.1°C; Ziegeweid et al. 2008), and the
lowest CTmax value was recorded from early life stage white
sturgeon (21.9°C; Earhart, Blanchard, Morrison, etal.2023). It
is important to note that the acclimation temperatures used in
each study varied based on the relative habitat of the sturgeon
species being investigated and thus reflective of their thermal
capacity in their native environment. Therefore, we also ran
a meta- regression analysis to assess acclimation temperature
as a moderator of CTmax (Table S2). We found acclimation
temperature was an important predictor of upper thermal
limits, explaining > 50% of the variation in CTmax (p < 0.0001;
R2marginal = 0.523; Figu re8a), where sturgeon at high acclima-
tion temperatures displayed higher upper thermal limits.
The overall meta- analytical mean for sturgeon thermal toler-
ance plasticity was statistically significantly different from zero
or no acclimation capacity (ARR = 0.563; CI = 0.3908, 0.7350;
p < 0.00 01; Table S2; Figure 7b). Though reported for only
three species, we found lake sturgeon (Figure7d; AR R = 0.474;
95% CI = 0.036, 0.913), shortnose sturgeon (ARR = 0.538; 95%
CI = 0.077, 0.998), and white sturgeon (ARR = 0.632; 95%
CI = 0.249, 1.015) all demonstrated substantial plasticity in
thermal tolerance. Experimental temperature was the only im-
portant moderator of ARR, where with increased experimental
temperature the magnitude of a sturgeon's plasticity in thermal
tolerance decreased (p < 0.0 001; R2marginal = 0.115; Ta ble S2;
Figure8b). Neither control temperature, temperature difference,
FIGUR E  | T he effect of temperature on the phys iological r ates of North American st urgeon. Overal l temperature- correcte d effect sizes (ln RRQ10)
and variation by metric for (a, b) activity, (c, d) growth , and (e, f) metabolism. Mean meta- analytical est imates (dark circles) with their 95% confidence
intervals (thick bars) and prediction inter vals (thin bars) are overlaid indiv idual data points (light circles) and scaled by precision (inverse of standard
error). An asterisk (*) represents an effect size that is significantly d ifferent from zero. k represents the number of effect sizes presented, and the value
in parentheses represents the total number of studies from which the effect sizes were calculated.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
10 of 24 Global Change Biology, 2024
acclimation duration, nor body mass were significant modera-
tors of ARR.
The high overall ARR for sturgeons was driven in part by high
ARRs from Earhart, Blanchard, Morrison, et al.(2023). These
individuals represent not only the highest ARRs recorded but
also the youngest sturgeon tested to date. Thus, we explored
whether age had a significant influence on ARR. There was no
significant relationship between age and ARR overall (Figure9;
p = 0.092; adjusted R2 = 0.097; n = 21); however, there was a well-
supported logistic relationship between age and ARR when fish
older than 400 days post- fertilization were excluded (p < 0.001;
adjusted R2 = 0.601; n = 18).
We also assessed sturgeon thermal plasticity by investigating if
they maintained TSM when acclimated to warm temperatures,
demonstrating perfect compensation for thermal stress. Here,
a slope of 0 indicates perfect compensation, and a slope of 1
indicates no plasticity. There was a significant negative linear
relationship between change in TSM and change in acclima-
tion temperatures (Figure 10a; p < 0.0 01; adjusted R2 = 0.42;
slope = 0.71; n = 22), suggesting that despite higher overall plas-
ticity indicated by ARR values, warm- acclimated sturgeon have
reduced thermal safety margins. There was also a significant
positive linear relationship between change in TSM and ARR
(Figure 10b; p < 0.001; adjusted R2 = 0.74; slope = 6. 36; n = 22).
This relationship again demonstrated the only instances of com-
plete acclimation, which coincided with improved thermal sa fety
margins, were for the youngest sturgeon tested to date from
Earhart, Blanchard, Morrison, et al. (2023). Though sturgeon
demonstrate higher overall ARR via increasing CTmax during
warm acclimation, this increase in CTmax still coincides with a
reduction in thermal safety margins (Figure10c). Interestingly,
there is a signif icant positive relationship between “natural” (i.e.,
control) CTmax and thermal safety margins (p < 0 .001; a djusted
R2 = 0.42; slope = 0.52; n = 22), but when fish were acclimated
to warm temperatures, they did not demonstrate a relationship
between CTmax and thermal safety margins (p = 0.962; adjusted
R2 = 0.05; slope = 0.01; n = 22) .
4 | Discussion
Understanding how warming affects sturgeon is critical for
predicting how these threatened and endangered species will
fare in a rapidly changing world. Here, we provide the first
comprehensive synthesis to characterize thermal effects, limits,
and plasticity across eight North American species, at multiple
life stages, and with regards to important ecological activities
(e.g., spawning, growth). Our data indicate sturgeon have the
capacity for thermal acclimation (though with some concern-
ing trends with energetic costs and survival) and impressive
plasticity in acute thermal tolerance, especially in the early life
stages. However, we acknowledge data gaps in the literature
limit overarching conclusions, and we highlight specific re-
search needs for conservation.
4.1 | Thermal Limits Vary by Habitat, Species, Life
Stage, and Metric
We predicted that given the diverse habitats sturge on occupy and
their vast ranges, there may be interspecific or even population-
level differences in thermal limits (e.g., Bugg et al. 2020).
Generally, the data collected from observational studies sug-
gest that the upper limit for presence and spawning for North
American sturgeon ranges between 20°C and 24°C. However,
we urge that this estimation be taken with caution, as there are
marked differences within and between species. For example,
juvenile Atlantic sturgeon are present in the Hudson River, New
York, at temperatures ranging from 0°C in the winter to 28°C in
the summer (Bain etal.2000). As such, it is exceedingly difficult
to provide an all- encompassing estimation due to the inherent
complexity of the data (i.e., reconciling methodological differ-
ences) and the lack of information for certain species, life stages,
and habitats. Instead, we suggest that the observational data
provided in TableS1 be used to inform future studies, or where
enough information exists to make inferences for a species, be
used for habitat- specific recommendations.
Similarly, physiological upper thermal limits reported here are
also likely to be driven in part by differences in life stages, hab-
itat temperatures, methodology, and data availability, making
overarching inferences difficult. Under natural conditions,
the overall upper thermal limit of North American sturgeon is
~30.3°C, which interestingly is double that of the average accli-
mation temperature for these data (14.8°C). This would indicate
that sturgeon have a large margin to buffer from changes in en-
vironmental temperature. However, we found individual ther-
mal safety margins vary drastically from 8°C to 18°C across life
stage, species, and habitat, likely because CTma x is particularly
dependent on the prevailing environmental temperature itself.
In fact, Zhang and Kieffer(2014) previously found the relation-
ship between CTmax and acclimation temperature is nonlinear
for shortnose sturgeon, where CTmax plateaus with increasing
acclimation temperature. Therefore, sturgeon become more
vulnerable with increased warming, despite increasing upper
thermal limits.
FIGUR E  | The effect of temperature on sur vival of early- life
stage North American sturgeon. Mean meta- analytical estimates (dark
circles) for log odds ratio (lnOR) with their 95% confidence intervals
(thick bars) and prediction intervals (thin bars) are overlaid individual
data points (light circles) and scaled by precision (inverse of standard
error). k represents the number of effect sizes presented, and the value
in parentheses represents the total number of studies from which the
effect sizes were calculated.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
11 of 24
Previous research has shown that freshwater and marine ecto-
therms decrease upper thermal limits with increasing habitat
latitude (Sunday, Bates, and Dulvy2011; Sunday et al.2019).
Some of the trends found here follow this assumption, but the
limited available data precludes a full assessment of whether
sturgeon thermal limits are inherently distinct across latitudes.
In one study based in Manitoba, northern la ke sturgeon demon-
strated lower thermal tolerance and acclimatory capacity than
their southern counterparts reared at the same temperatures
(Bugg etal.2020). Yet in most cases, comparisons across stud-
ies are confounded by different rearing temperatures and/
or natural conditions. For example, shortnose sturgeon and
Atlantic sturgeon occupy similar habitat ranges and demon-
strate similar upper thermal limits (Figure 7). However, re-
ports of Atlantic sturgeon thermal tolerance under control
conditions are limited to two studies from New Brunswick,
Canada (Spear and Kieffer 2016; Penny etal. 2023), whereas
reports of shortnose sturgeon thermal tolerance range from
New Brunswick (acclimated to 10°C; Zhang and Kieffer2014)
to Georgia, USA (acclimated to 24°C; Ziegeweid etal. 2008).
Thus, shortnose sturgeons display a much wider range of ther-
mal limits, likely as an artifact of data availability. Likewise,
white sturgeon are widely distributed on the western coast
of North America and, at lower latitudes, share habitat with
FIGUR E  | Variation in the natural upper thermal limits and thermal tolerance plasticity across North A merican sturgeon species. (a) Overall
upper thermal limits when acclimated to natural (i.e., control) temperatures for five of the eight species in this study; (b) variation in upper thermal
limits across species; (c) overall level of plasticity in heat tolerance, as calculated by acclimation response ratios (ARRs); and (d) variation in thermal
tolerance plasticity across species. Mean meta- analytical estimates (dark circles) with their 95% confidence intervals (thick bars) and prediction
intervals (thin bars) are overlaid individual data points (light circles) and scaled by precision (inverse of standard error). For (c, d), the gray dashed
line at 0 indicates no capacity for thermal acclimation, whereas ARR of 1 indicates full compensation. k represents the number of effect sizes
presented, and the value in parentheses represents the total number of studies from which the effect sizes were calculated.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
12 of 24 Global Change Biology, 2024
green sturgeon. Supporting the relationship between ecto-
therm thermal limits and latitude, green sturgeon demonstrate
significantly higher thermal tolerance than white sturgeon
(Figure 7). However, data for white sturgeon includes that of
early life stages (~15 dpf), which have a considerably lower
CTmax than older life stages when acclimated to 14°C (Earhart,
Blanchard, Morrison, etal.2023).
Dahlke etal.(2020) suggested that embryos and spawning fish
have narrower thermal margins and are therefore more vulnera-
ble to climate warming than larvae, juveniles, and nonreproduc-
tive adults. Little data exist within or across species to confirm
whether a thermal bottleneck exists for sturgeon at different life
stages, and any ontogenetic differences may be confounded by
methodological differences in thermal tolerance measurements
(Pottier et al. 2022). As demonstrated here, CTma x studies are
dominated by the use of the YOY life stage, whereas survival
studies and observational studies are more common for early life
and juveniles/adults, respectively. The only species for which
thermal tolerance of more than two life stages is reported, using
consistent methodology, are white sturgeon. The upper ther-
mal limit of white sturgeon acclimated to 14°C and challenged
with a temperature increase of 0.3°C/min increases from early
life (yolk sac larvae; 21.9°C; Earhart, Blanchard, Morrison,
et al. 2023) to YOY (28.2°C; Earhart, Blanchard, Strowbridge,
etal.2023) to the juvenile stage (29.8°C; Weber, Dichiera, and
Brauner2024). These data in white sturgeon do indeed suggest
that earlier life stages are more sensitive to warming, at least
within early development and the first years of life. However,
there are no studies of CTmax on spawning- capable or actively
spawning adults of any sturgeon species, certainly due to the
logistical and ethical challenges of working with large- bodied,
endangered animals. Studies with well- defined and consistent
methodology are urgently needed to investigate how both life
stage and habitat may underpin differences in sturgeon upper
thermal limits, but we recognize the difficulty of reconciling
FIGUR E  | Upper thermal limits and thermal tolerance plasticity as a function of acclimation or experimental temperature. (a) Acclimation
temperature (°C) was a significant moderator of upper thermal limits under “natural” conditions, measured as critical thermal maxima (CTmax ;
p < 0.00 01; R2marginal = 0.523), and (b) experiment temperature (°C) was a significant moderator of thermal tolerance plasticity, measured as
acclimation response ratio (ARR; p < 0 .0001; R2marginal = 0.115). For both, models reported significant residual heterogeneity (p < 0.00 01), and
therefore, there remain unknown sources of variance for CTmax and ARR .
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
13 of 24
the disconnect between field- based, ecological thermal limits
and acute upper thermal limits. To expand our understanding
of how thermal limits change across lifespans, we must become
creative in our methodology, connecting lab- based techniques to
measure more conservative thermal thresholds (e.g., avoidance
behavior, slow ramping rates for CTmax) and field- based tech-
niques to more precisely measure invivo thermal preferences
and limits (e.g., implantable thermal profile tags).
4.2 | Prolonged Temperature May Have
Concerning Impacts on Whole- Animal Physiology
After prolonged exposure to temperature change, sturgeon gener-
ally display similar physiological responses as they would under
control or “natural” conditions, suggesting a strong capacity for
acclimation. However, there are trends where metabolism, and
specifically standard or basal metabolic rate, increase with pro-
longed temperature, indicating increased maintenance costs. This
is unsurprising, as temperature is known to have a profound effect
on biological processes such as ox ygen consumption (Schulte2015;
Alfonso, Gesto, and Sadoul2021). However, the pairwise compar-
isons we chose to use here, between control and acclimated condi-
tions, can obscure the overall pattern of thermal effects. Primarily,
without quantifying how acute temperature change affects stur-
geon physiology, we have a limited understanding of the thermal
plasticity they employ during acclimation. There are few instances
of acute responses to temperature (e.g., Kieffer etal. 2014); how-
ever, more complex factorial experiments are needed to address
whether the responses found with prolonged acclimation indicate
active or passive thermal plasticity and the degree to which these
fish may be compensating for thermal stress (Havird etal.2020).
In addition, in many cases performance plateaus and/or declines
with increasing temperature, suggesting a thermal threshold has
been reached (Angilletta2009; Schulte, Healy, and Fangue2011;
Schu lte 2014, 2015; Jeffries, Fangue, and Connon 2018). For ex-
ample, in pallid sturgeon, metabolism increases with temperature
when acclimated between 13°C and 25°C, but not between 25°C
and 28°C (Chipps, Klumb, and Wright2010). This suggests a ther-
mal limit on metabolic performance that is not conveyed through
the effect size calculation. Previous studies have also found species
FIGUR E  | Relationship between acclimation response ratio
and age (days post- fertilization) of North American sturgeon species
combined. There is poor support for an overall relationship between
ARR and all ages (n = 22). However, within ~1 year of life (n = 19), there
is a logarith mic relationship between A RR and age (shown in ins et). The
dashed line and surrounding gray area indicate logarithmic regression
and a 95% confidence interval and are overlaid with individual data
points.
FIGURE  | Legend on next page.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
14 of 24 Global Change Biology, 2024
and even populations demonstrate variable metabolic responses to
warming, for example, increasing with warming (shortnose stur-
geon; Zhang and Kieffer2014) or decreasing (e.g., lake sturgeon;
Bugg etal.2020). For these reasons, when assessing temperature
limits in young sturgeon, species- and even population- specific
thermal performance curves, rather than pairwise comparisons,
are necessary to properly understand thermal effects and limita-
tions of growth and activity.
Our data also suggest warmer temperatures and longer dura-
tions of warming may inhibit growth, which is concerning as
size can be one of the largest determinants of survival during
this first year of life, when predation is often high (Justice
et al. 2009; Caroffino et al. 2010; Hardy et al. 2021). Across
species, sturgeon appear to maintain growth in warm tempera-
tures, sometimes at the cost of other physiological processes or
performance (Earhart, Blanchard, Morrison, etal.2023; Hung
etal.1993; Allen, Nicholl, etal.2006; Kappenman etal.2009;
Boucher, McAdam, and Shrimpton 2 014; Poletto et al. 2018;
Bugg et al. 2020; Brandt et al.2022), and in spite of predation
risks (Bjornson, Earhart, and Anderson2020). However, it is im-
portant to note these assessments are based on sturgeon reared
in laboratory environments with abundant food availability. For
example, when larval green sturgeon were fed optimally, fish ex-
hibited the highest relative condition under warming; however,
when food was limited, warm- acclimated fish had the poorest
condition (Poletto etal.2018). In natural environments, if food
limitation co- occurs with elevated temperatures, increased met-
abolic demands may decrease growth and further exacerbate
impairments to physiological rates.
In addition, we found decreases in survival even in controlled lab-
oratory settings with minimal compounding stressors. As such,
when extrapolating findings from controlled settings to natural
habitats, it is important to consider how the differences in these
environments may impact our interpretations of success or failure
under warming. Decreases in immune capacity, changes in gene
expression associated with stress, reductions in aerobic capacity,
and higher mortality have all been reported while YOY sturgeon
continue to grow under warm temperatures (Bugg et al. 2020,
2023; Earhart, Blanchard, Morrison, etal.2023). Thus, it is likely
that the impacts of increasing temperatures have an overall neg-
ative effect on sturgeon, particularly in early life stages, which is
especially concerning as the recruitment and survival of early life
stages of sturgeon are one of their leading conservation obstacles
(Anderson, Schreier, and Crossman2022).
4.3 | North American Sturgeon Have Greater
Acclimation Capacity Than Other Fishes
Here, we found North American sturgeon have a greater ca-
pacity for thermal acclimation on average than previously
described for other fishes and can increase their thermal lim-
its at a mean of 0.56°C per 1°C acclimation (Figure 8). While
aquatic ectotherms have been found to have more than twice
the thermal tolerance plasticity of terrestrial ectotherms in late
life stages (Gunderson and Stillman2015; Ruthsatz etal.2024)
and more than three times the thermal tolerance plasticity of
terrestrial ectotherms during development (Pottier etal.2022),
previously reported average ARRs are typically < 0.4. This ca-
pacity for thermal tolerance plasticity is somewhat surprising
as, in general, sturgeon have demonstrated reduced responses
to physiological stressors (e.g., hypoxia, salinity, exhaustive ex-
ercise) in comparison to other fishes (e.g., Kieffer etal. 2014;
Baker, Wood, and Kieffer 2005; Penny and Kieffer 2019). It
should be noted that only three species of North American
sturgeon have been characterized thus far, and more ARR data
is needed to understand if this is truly an Acipenseriformes
trait or a result of polyploidy across sturgeon. More research
is needed to test whether ploidy differences between sturgeon
and other fish could explain differences in acclimation capac-
ity. However, it is an encouraging find that indicates sturgeon
species may have an acclimatory advantage and, importantly,
can better offset changes to their thermal safety margins under
warming scenarios.
Notably, early- life stage sturgeon demonstrated near- perfect
or even overcompensation of thermal acclimation (Earhart,
Blanchard, Morrison, etal.2023). This elevated capacity for accli-
mation exponentially declines in the first year of life (Fig ure9), but
importantly, even with the exclusion of early life stages, sturgeon
overall maintain elevated capacity for thermal acclimation. This
pattern contrasts recent studies in embryonic stages that show
reductions in thermal tolerance at high acclimation temperatures
and low or non- adaptive plasticity (Dahlke et al. 2020; Pottier
etal.2022). This increased plasticity during early life may be ex-
ceptionally critical for a species with long generation times like the
sturgeon (Earhart, Blanchard, Morrison, etal.2023). However, it is
important to note that the early life stages reported here are yolk-
sac larvae, and as such, it is possible that embryonic life stages are
less plastic than their hatched counterparts. Finally, data beyond
the three reports for sturgeon > 400 days old are needed to investi-
gate this potential connection between ontogeny and acclimation
capacity and to better understand the impacts of elevated tempera-
tures on adult physiology and spawning.
Yet even with their impressive thermal acclimation capac-
ity, sturgeon do display limits to this tolerance. Earhart,
Blanchard, Morrison, etal.(2023) reported a decrease in ARR
between subsequent acclimations for early- life white sturgeon,
and other sturgeon species similarly demonstrate a nonlin-
ear relationship, resulting in a decline in acclimation capac-
ity under higher temperatures (Bugg et al. 2020; Zhang and
FIGURE  | Relationship between upper thermal limits, plasticity
in heat tolerance, and thermal safety margins of North American
sturgeon. (a) Changes in thermal safety margin given changes in
acclimation temperature, where a slope of 0 demonstrates perfect
compensation and a slope of 1 demonstrates no plasticity. (b) Changes
in thermal safety margin given changes in acclimation response ratio,
where a thermal safety margin of 0 demonstrates perfect compensation
and an accli mation response ratio of 1 demonstrat es perfect acclim ation.
(c) Differences in the relationship between critical thermal maxima
and thermal safety margin based on acclimation treatment (control
represented in blue and warm acclimation represented in red). The
dashed line and surrounding gray area indicate linear regression and
a 95% confidence interval and are overlaid with individual data points
(light circles).
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
15 of 24
Kieffer2014). Any decrease in ARR is inherently accompanied
by a reduction in thermal safety margin (Figure10), increasing
sturgeon's vulnerability to warming. While the reported ARRs
here are calculated between control temperatures and warm
acclimations, we must acknowledge that characterizing the
limits of an organism's acclimation capacity across multiple,
increasing acclimation temperatures is likely more valuable
for understanding how species will be impacted by warming
than pairwise comparisons alone.
4.4 | Implications and Future Research Needs
for Sturgeon Success in the Face of Climate Change
As sturgeon are long- lived species with relatively few genomic
changes occurring through millions of years of evolution
(Brownstein et al.2024), individuals likely rely on their abil-
ity to acclimate to environmental changes in real time, which
necessitates their impressive plasticity in the face of increased
environmental temperatures. During early development, stur-
geon appear to have higher acclimation capacities compared
to later life stages, which may aid during a period of limited
mobility when effective behavioral thermoregulation (e.g.,
swimming far distances to avoid high temperatures) is not
feasible (Allen, Hodge, etal.2006; Verhille etal.2 014; Brandt
etal.2021). However, early life stages are also more vulnera-
ble to mortality with warming, with yolk- sac larvae especially
susceptible (Earhart, Blanchard, Morrison, et al. 2023). This
suggests that thermal plasticity may be inversely related to ther-
mal sensitivity in sturgeons. For juvenile and adult life stages,
critical temperatures for presence and spawning are typically
much lower than CTmax, suggesting that while sturgeon may
be able to withstand these temperatures acutely in a laboratory
trial, in their natural habitat, they favor behavioral thermo-
regulation to reduce the temperatures that they are exposed to
(e.g., Breece etal.2016; Jetter, Crossman, and Martins2023).
While beneficial for mitigating mortality, behavioral thermo-
regulation can also lead to abandonment of spawning grounds
if environmental temperatures exceed thresholds, similar to
spawning ground abandonment seen during periods of sub-
optimal flow rates (Paragamian and Kruse 20 01). This would
then reduce reproductive success and limit future recruit-
ment. Conversely, behavioral thermoregulation can be limited
during extreme summer temperatures (Moore, Paukert, and
Moore2021), which may prove quite challenging for sturgeons
to cope with and require reliance on physiological thermal
plasticity. With this delicate balance between movement and
habitat occupancy, there is a great need to identify, protect, and
promote access to areas of thermal refuge (Sullivan, Jager, and
Myers2003; Caissie2006; Amat- Trigo etal.2023) during peri-
ods where environmental temperatures exceed the sturgeon's
thermal capacity.
Critically, more studies investig ating the physiological impacts of
warming are needed for almost all life stages of North American
sturgeon, but especially in combination with co- occurring
stressors, as these impacts are predicted to be more challenging
for fish to cope with than warming alone (Earhart etal.2022).
To assist with future sturgeon conservation research, we have
identified the following data gaps and provided areas for future
research:
1. How do thermal effects, limits, and plasticity change with
age? Different life stages are inherently more suitable for
certain metrics, where laboratory- based experiments favor
small- bodied individuals and field measurements allow the
investigation of large adults. However, siloing thermal as-
sessments by which measurements are easiest to perform
for each life stage hinders our understanding of how vul-
nerability changes with ontogeny. The free- embryo (YSL)
and feeding stage are known to be the most stressful part of
a sturgeon's development (e.g., highest mortality and large
morphometric changes), yet there is only one thermal tol-
erance study conducted at this life stage. In addition, only
three studies included in the effect size and thermal toler-
ance plasticity analyses were conducted on sturgeon past
the first year of life. If not space- , time- , or cost- prohibitive,
experimental work with life stages outside the YoY group
would provide useful vulnerability assessments.
2. What is the relationship between measures of lab- based
thermal tolerance and plasticity and habitat utilization?
Thermal tolerance has only been measured for five species
of sturgeon, and acclimation capacity has only been charac-
terized for three. Paired with the limited information on life
stage- specific characterizations, we do not yet have enough
data to understand how lab- based measures of thermal
tolerance translate into habitat preference and avoidance.
While we know that there is the potential for population-
specific thermal plasticity (Bugg et al. 2020, 2023), more
evaluations are needed, especially for populations of con-
cern, to best inform management efforts. Including studies
on avoidance and escape behavior in the lab, as well as sen-
sitive thermal profiles via implantable temperature loggers
in the field, could help reconcile the difference between lab-
and field- based measurements. In addition, bioindicators of
thermal stress, particularly those obtained using non- lethal
sampling methods (e.g., blood samples for biochemical
stress markers and transcriptomics; Spear and Kieffer2016;
Penny etal.2023) are a promising avenue for comparative
analyses, connecting physiology in the lab and field.
3. How do sturgeon cope with stressors representative of the
natural environment (in duration, magnitude, variation,
predictability, asynchrony, etc.)? Climate change stresses
do not act individually, and co- occurring stressors will con-
tinue to be more severe as global warming progresses. Yet,
multi- stressor studies conducted on sturgeon are scarce,
and the few that have assessed the impacts of warming with
an additional stressor exhibit variable responses. Long- term
studies that evaluate the impacts of prolonged exposures
to elevated temperatures, or those that are repeated across
years, are few and far between. Furthermore, differences
in thermal history profiles may arise in the wild depending
on the timing of spawning and how that aligns with sea-
sonal changes, but little is known about the impact of early
life exposure on thermal tolerance and plasticity. Thus, it
is difficult to predict the physiological impacts of chronic
and repeated temperature increases associated with climate
change. Together, despite their notable plasticity, uncer-
tainty still remains concerning the fate of sturgeons as cli-
mate change intensifies, and physiological impacts across
life stages likely limit their survival and long- term repro-
ductive potential.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
16 of 24 Global Change Biology, 2024
Author Contributions
Angelina M. Dichiera: conceptualization, data curation, formal
analysis, investigation, methodology, visualization, writing – original
draft. Madison L. Earhart: data curation, investigation, visualization,
writing – original draft. Will iam S. Bugg: data curation, investigation,
writing – original draft. Colin J. Brauner: funding acquisition, project
administration, resources, supervision, writing – review and editing.
Patricia M. Schulte: funding acquisition, project administration, re-
sources, supervision, writing – review and editing.
Conflicts of Interest
The authors declare no conflicts of interest.
Data Availability Statement
The data that support the findings of this study are openly available in
figshare at: https:// figsh are. com/ proje cts/ Meta- analy tical_ review_ of_
the_ therm al_ toler ance_ and_ adapt ive_ capac ity_ of_ North_ Ameri can_
sturg eon/ 201795.
References
Alfonso, S., M. Gesto, and B. Sadoul. 2021. “Temperature Increase and
Its Effects on Fish Stress Physiology in the Context of Global Warming.”
Journal of Fish Biology 98, no. 6: 1496 –1508.
Allen, P. J., B. Hodge, I. Werner, and J. J. Cech Jr. 2006. “Effects of
Ontogeny, Season, and Temperature on the Swimming Performance of
Juvenile Green Sturgeon (Acipenser medirostris).” Canadian Journal of
Fisheries and Aquatic Sciences 63, no. 6: 1360–1369.
Allen, P. J., M. Nicholl, S. Cole, A. Vlazny, and J. J. Cech. 2006. “Growth
of Lar val to Juvenile Green Stu rgeon in Elevated Temperatu re Regimes.”
Transactions of the American Fisheries Society 135: 89–96.
Amat- Trigo, F., D. Andreou, P. K. Gillingham, and J. R. Britton. 2023.
“Behavioural Thermoregulation in Cold- Water Freshwater Fish: Innate
Resilience to Climate Warming?Fish and Fisheries 24, no. 1: 187–195.
Anderson, W. G., A. Schreier, and J. A. Crossman. 2022. “Conser vation
Aquaculture—A Sturgeon Story.” In Fish Physiology, vol. 39, 39–109.
Cambridge, M A: Academic Press.
Angi lletta, M. J. 200 9. Thermal Adaptati on: A Theoretical an d Empirical
Synthesis. New York; Oxford, UK: Oxford University Press.
Araújo, M. B., F. Ferri- Yáñez, F. Bozinovic, P. A. Marquet, F. Valladares,
and S. L. Chown. 2013. “Heat Freezes Niche Evolution.” Ecology Letters
16: 1206–1219.
Bain, M., N. Haley, D. Peterson, J. R. Waldman, and K. A rend. 2000.
“Harvest and Habitats of Atlantic Sturgeon Acipenser oxyrinchus
Mitchill, 1815 in the Hudson River Estuary: Lessons for Sturgeon
Conservation.” Boletin- Instituto Espanol De Oceanografia 16, no. 1/4:
43–54.
Baker, D. W., A. M. Wood, and J. D. Kieffer. 2005. “Juvenile Atlantic
and Shortnose Sturgeons (Family: Acipenseridae) Have Different
Hematological Responses to Acute Environmental Hypoxia.”
Physiological and Biochemical Zoology 78, no. 6: 916–925.
Baril, A. M., J. T. Buszkiewicz, P. M. Biron, Q. E. Phelps, and J. W. A.
Grant. 2018. “Lake Sturgeon (Acipenser fulvescens) Spawning Habitat:
A Quantitative Review.” Canadian Journal of Fisheries and Aquatic
Sciences 75: 925–933.
Beaman, J. E., C. R. White, and F. Seebacher. 2016. “Evolution of
Plasticity: Mechanistic Link Between Development and Reversible
Acclimation.” Trends in Ecology & Evolution 31: 237–249.
Bemis, W. E., E. K. Findeis, and L. Grande. 1997. “An Overview of
Acipenseriformes.” Environmental Biology of Fishes 48: 25–71.
Bennett, J. M., J. Sunday, P. Calosi, etal. 2021. “T he Evolution of Critical
Thermal Limits of Life on Earth.” Nature Communications 12: 1198.
Bjornson, F., M. Earhart, and W. G. Anderson. 2020. “To Feed or Flee:
Early Life- History Behavioural Strategies of Juvenile Lake Sturgeon
(Acipenser Fulvescens) During R isk- Sensitive Foraging.” Canadian
Journal of Zoology 98, no. 8: 541–550.
Boucher, M. A., S. O. McAdam, and J. M. Shrimpton. 2014. “The
Effect of Temperature and Substrate on the Growth, Development and
Survival of Larval White Sturgeon.” Aquaculture 430: 139 –148.
Brandt, C., W. Bugg, L . Groening, C. K lassen, and W. G. Anderson. 20 21.
“Effects of Rearing Temperature on Volitional and Escape Response
Swimming Performance in Lake Sturgeon, Acipenser fulvescens, From
Hatch to Age 1.” Environmental Biology of Fishes 104, no. 7: 737–750.
Brandt, C., L. Groening, C. Klassen, and W. G. Anderson. 2022.
“Effects of Rearing Temperature on Yolksac Volume and Growth Rate
in Lake Sturgeon, A. fulvescens, From Hatch to Age- 1.” Aquaculture
546: 737352.
Breece, M. W., D. A. Fox, K. J. Dunton, M. G. Frisk, A. Jordaan, and
M. J. Oliver. 2016. “Dynamic Seascapes Predict the Marine Occurrence
of an Endangered Species: Atlantic Sturgeon Acipenser oxyrinchus
Oxyrinchus.” Methods in Ecology and Evolution 7, no. 6: 725–733.
Breece, M. W., D. A. Fox, D. E. Haulsee, I. I. Wirgin, and M. J. Oliver.
2018. “Satellite Driven Distribution Models of Endangered Atlantic
Sturgeon Occurrence in the Mid- Atlantic Bight.” ICES Journal of
Marine Science 75, no. 2: 562–571.
Brown, K. 2007. “Evidence of Spawning by Green Sturgeon, Acipenser
medirostris, in the Upper Sacramento River, California.” Environmental
Biology of Fishes 79: 297–303.
Brownstein, C. D., D. J. MacGuigan, D. Kim, etal. 2024. “The Genomic
Signatures of Evolutionary Stasis.” Evolution 78, no. 5: 821–834.
Bugg, W. S., G. R. Yoon, A. N . Schoen, etal. 20 20. “Effect s of Acclimation
Temperature on the T hermal Physiology in Two Geogr aphically Distinct
Populations of Lake Sturgeon (Acipenser fulvescens).” Conser vation
Physiology 8: coaa087.
Bugg, W. S., G. R. Yoon, A. N. Schoen, A. M. Weinrauch, K. M. Jeffries,
and W. G. Anderson. 2023. “Elevated Temperatures Dampen the Innate
Immune Capacity of Developing Lake Sturgeon (Acipenser fulvescens).”
Journal of Experimental Biology 226: jeb245335.
Burkhead , N. M. 2012. “Ext inction Rates in North A merican Freshwat er
Fishes, 1900–2010.” Bioscience 62: 798–808.
Caissie, D. 2 006. “T he Thermal Regi me of Rivers: A Review.” Freshwater
Biology 51, no. 8: 1389–1406.
Campos, D. F., R. D. Amanajás, V. M. Almeida- Val, and A. L. Val. 2021.
“Climate Vulnerability of South American Freshwater Fish: Thermal
Tolerance and Acclimation.” Journal of Experimental Zoolog y Part A:
Ecological and Integrative Physiology 335, no. 9- 10: 723–734.
Caroffino, D. C., T. M. Sutton, R. F. Elliott, and M. C. Donofrio. 2010.
“Early Life Stage Mortality Rates of Lake Sturgeon in the Peshtigo
River, Wisconsin.” North American Journal of Fisheries Management
30, no. 1: 295–304.
Caron, F., D. Hatin, and R. Fortin. 2002. “Biological Characteristics
of Adult Atlantic Sturgeon in the St Lawrence River Estuary and the
Effectiveness of Management Rules.” Journal of Applied Ichthyology 18,
no. 4–6: 580–585.
Carr, S. H., F. Tatman, and F. A. Chapman. 1996. “Obser vations on the
Natural History of the Gulf of Mexico Sturgeon (Acipenser oxyrinchus
de sotoi Vladykov 1955) in the Suwannee River, Southeastern United
State s.” Ecology of Freshwater Fish 5, no. 4: 169–174.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
17 of 24
Chapman, F. A., and S. H. Carr. 1995. “Implications of Early Life Stages
in the Natural History of the Gulf of Mexico Sturgeon, Acipenser oxyr in-
chus de sotoi.” Environmental Biology of Fishes 43: 407–413.
Chipps, S. R ., R. A. Klumb, and E. B. Wright. 2010. “Development and
Application of Juvenile Pallid Sturgeon Bioenergetics Model.” Final
Report to South Dakota Department of Game, Fish and Parks, Federal
aid Project Number T- 24- R: 2424.
Claussen, D. L. 1977. “Thermal Acclimation in Ambystomatid
Salamanders.” Comparative Biochemistry and Physiolog y, Part A:
Molecular & Integrative Physiology 58: 333–340.
Comte, L., L . Buisson, M. Dauf resne, and G. Grenouillet. 2 013. “Climate-
Induced Changes in the Distribution of Freshwater Fish: Obser ved and
Predicted Trends.Freshwater Biology 58: 625–639.
Comte, L., and J. D. Olden. 2017. “Evolutionary and Environmental
Determinants of Freshwater Fish Thermal Tolerance and Plasticity.”
Global Change Biology 23, no. 2: 728–736.
Cooke, S. J., L. Sack, C. E. Franklin, etal. 2013. “W hat Is Conservation
Physiology? Perspectives on an Increasingly Integrated and Essential
Science.” Conservation Physiology 1: cot001.
Dadswell, M. J. 1979. “Biology and Population Characteristics of the
Shortnos e Sturgeon , Acipenser brevirost rum LeSue ur 1818 (Osteichthyes:
Acipenseridae), in the Saint John River Estuar y, New Brunswick,
Canada.” Canadian Journal of Zoology 57, no. 11: 2186–2210.
Dahlke, F. T., S. Wohlrab, M. Butzin, and H. O. Pörtner. 2020. “Thermal
Bottlenecks in the Life Cycle Define Climate Vulnerability of Fish.”
Science 369, no. 6499: 65–70.
Dammerman, K. J., J. P. Steibel, and K. T. Scribner. 2016. “Increases
in the Mean and Variability of Thermal Regimes Result in Differential
Phenotypic Responses Among Genotypes During Early Ontogenetic
Stages of Lake Sturgeon (Acipenser fulvescens).” Evolutionary
Applications 9, no. 10: 1258–1270.
Desforges, J. E., K. Birnie- Gauvin, F. Jutfelt, etal. 2023. “The Ecological
Relevance of Critical Thermal Maxima Methodology for Fishes.”
Journal of Fish Biology 102, no. 5: 1000–1016.
Dudgeon, D., A. H. Arthington, M. O. Gessner, etal. 2006. “Freshwater
Biodiversity: Importance, Threats, Status and Conservation
Challenges.Biological Reviews 81: 163–182.
Earhart, M. L., T. S. Blanchard, A. A. Harman, and P. M. Schulte. 2022.
“Hypoxi a and High Temperature as Inter acting Stressor s: Will Plasticity
Promote Resilience of Fishes in a Changing World?” Biological Bulletin
243, no. 2: 149–170.
Earhar t, M. L., T. S. Blanchard , P. R. Morris on, etal. 2023 . “Identification
of Upper Thermal Thresholds During Development in the Endangered
Nechako White Sturgeon With Management Implications for a
Regulated River.” Conservation Physiology 11: coad032.
Earhart, M. L., T. S. Blanchard, N. Strowbridge, etal. 2023. “Heatwave
Resilience of Juvenile White Sturgeon Is Associated With Epigenetic
and Transcriptional Alterations.” Scientific Reports 13: 15451.
Elliott, C. M., A. J. DeLonay, K. A. Chojnacki, and R. B. Jacobson. 2020.
“Characterization of Pallid Sturgeon (Scaphirhynchus albus) Spawning
Habitat in the Lower Missour i River.” Journal of Applied Ichthyol ogy 36,
no. 1: 25–38.
Erickson, D. L., and M. A. Webb. 2007. “Spawning Periodicity,
Spawning Migration, and Size at Maturity of Green Sturgeon, Acipenser
Medirostris, in the Rogue River, Oregon.” Environmental Biology of
Fishes 79: 255–268.
Flinders, C., and P. Wiegand. 2014. “Life History, Water Quality,
and Habitat Needs of Sturgeon Species: A Literature Review: NCASI
Technical Bulletin no. 1021.”
Fontana, F., R. M. Bruch, F. P. Binkowski, et al. 2004. “Karyotype
Charact erization of the Lake Stu rgeon, Acipenser fulvesc ens (Rafi nesque
1817) by Chromosome Banding and Fluorescent InSitu Hybridization.”
Genome 47, no. 4: 742–746.
Fry, F. 1947. Effects of the Environment on Animal Activit y. Vol. 55, 1–62.
Toronto: University of Toronto Press.
Fuller, D. B., M. E . Jaeger, and M. Webb. 200 8. Spawning and Ass ociated
Movement Patterns of Pallid Sturgeon in the Lower Yellowstone River
Upper Basin Pa llid Sturgeon Recover y Workgroup 20 07 Annual Report.
Upper Basin Workgroup, US Fish and Wildlife Service, Bozeman.
Gunderson, A. R., and J. H. Stillman. 2015. “Plasticity in Thermal
Tolerance Has Limited Potential to Buffer Ectotherms From Global
Warmi ng .” Proceedings of the Royal Society B: Biological Sciences 282:
20150401.
Hager, C. H., J. C. Watter son, and J. E. Kah n. 2020. “S pawning Driv ers and
Frequency of Endangered Atlantic Sturgeon in the York River System.”
Transactions of the American Fisheries Society 149, no. 4: 474–485.
Hardy, R. S., V. Zadmajid, I. A. Butts, and M. K. Litvak. 2021. “Growth,
Survivorship, and Predator Avoidance Capability of Larval Shortnose
Sturgeon (Acipenser brevirostrum) in Response to Delayed Feeding.”
PLoS One 16, no. 3: e0247768.
Havelka, M., V. Kašpar, M. Hulák, and M. Flajšhans. 2011. “Sturgeon
Genetics and Cytogenetics: A Review Related to Ploidy Levels and
Interspecific Hybridization.” Folia Zoologica 60: 93 –103.
Havird, J. C., J. L. Neuwald, A. A. Shah, A. Mauro, C. A. Marshall, and
C. K. Ghalambor. 2020. “Distinguishing Between Active Plasticity due
to Thermal Acclimation and Passive Plasticity due to Q10 Effects: Why
Methodolog y Matters.” Functional Ecolog y 34, no. 5: 1015–1028.
Haxton, T. J., and T. M. Cano. 2016. “A Global Perspective of
Fragmentation on a Declining Taxon the Sturgeon (Acipenseri formes).”
Endangered Species Research 31: 203–210.
Haxton, T. J., K. Sulak, and L. Hildebrand. 2016. “Status of Scientific
Knowledge of Nor th American Stu rgeon.” Journal of Applied Ich thyology
32: 5 –10.
Hilton, E. J., B. Kynard, M. T. Balazik, A. Z. Horodysky, and C. B.
Dillman. 2016. “Review of the Biology, Fisheries, and Conser vation
Status of the Atlantic Sturgeon (Acipenser oxyrinchus oxyrinchus
Mitchill, 1815).” Journal of Applied Ichthyology 32: 30–66.
Hildebrand, L. R., A. Drauch Schreier, and K. Lepla. 2016. “Status of
White Sturgeon (Acipenser transmontanusR ichardson, 1863) through-
out the species range, threats to survival, and prognosis for the future.”
Journal of Applied Ichthyology 32: 261–312. Portico. https:// doi. org/ 10.
1111/ jai. 13243 .
Hung, S. S., P. B. Lutes, A. A. Shqueir, and F. S. Conte. 1993. “Effect
of Feeding Rate and Water Temperature on Growth of Juvenile White
Sturgeon (Acipenser transmontanus).” Aquaculture 115, no. 3- 4:
297–3 03.
Ingram, E. C., and D. L. Peterson. 2018. “Seasonal Movements of
Shortnose Sturgeon (Acipenser brevirostrum) in the Altamaha R iver,
Georgia.” River Research and Applications 34, no. 7: 873–882.
IUCN. 2022. The IUCN Red List of Threatened Species. Version 2022- 2.
Jackson, Z. J., J. J. Gruber, and J. P. Van Eenennaam. 2016. “White
Sturgeon Spaw ning in the San Joaquin River, California, and Effects
of Water Management.” Journal of Fish and Wildlife Management 7, no.
1: 17 1–180.
Jeffries, K. M., N. A. Fangue, and R. E. Connon. 2018. “Multiple Sub-
Lethal Thresholds for Cellular Responses to Thermal Stressors in an
Estuarine Fish.” Comparative Biochemistry and Physiology Part A:
Molecular & Integrative Physiology 225: 33–45.
Jetter, C. N., J. A. Crossman, and E. G. Martins. 2023. “Movement
Behaviour of Endangered White Sturgeon Acipenser transmontanus
Responds to Changing Environmental Conditions Below a Dam.”
Endangered Species Research 50: 295–309.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
18 of 24 Global Change Biology, 2024
Justice, C., B. J. Pyper, R. C. Beamesderfer, et al. 2009. “Evidence of
Density- and Size- Dependent Mortality in Hatchery- Reared Juvenile
White Sturgeon (Acipenser transmontanus) in the Kootenai River.”
Canadian Journal of Fisheries and Aquatic Sciences 66, no. 5: 802–815.
Kappenman, K. M., W. C. Fraser, M. Toner, J. Dean, and M. A. Webb.
2009. “Effect of Temperature on Growth, Condition, and Survival of
Juvenile Shovelnose Sturgeon.” Transactions of the American Fisher ies
Society 138, no. 4: 927–937.
Kappenman, K. M., M. A. H. Webb, and M. Greenwood. 2013. “The
Effect of Temperature on Embryo Surv ival and Development in Pallid
Sturgeon Scaphirhynchus albus (Forbes & Richardson 1905) and
Shovelnose Sturgeon S. platorynchus (Rafinesque, 1820).” Journal of
Applied Ichthyology 29, no. 6: 1193–1203.
Kennedy, A. J., T. M. Sutton, and B. E. Fisher. 2006. “Reproductive
Biology of Female Shovelnose Sturgeon in the Upper Wabash River,
Ind iana .” Journal of Applied Ichthyology 22, no. 3: 177–182.
Kieffer, J. D., F. M. Penny, and V. Papadopoulos. 2014. “Temperature
has a reduced effect on routine metabolic rates of juvenile shortnose
sturgeon (Acipenser brevirostrum).” Fish Physiology and Biochemistr y
40, no. 2: 551–559. https:// doi. org/ 10. 10 07/ s1069 5 - 013- 9865- 8.
Knight, C. A., N. A. Molinari, and D. A. Petrov. 2005. “The Large
Genome Constraint Hypothesis: Evolution, Ecology and Phenotype.”
Annals of Botany 95, no. 1: 177–190.
Moore, M. J., C. P. Paukert, and T. L. Moore. 2021. “Effects of Latitude,
Season, and Temperature on Lake Sturgeon Movement.” North
American Journal of Fisheries Management 41, no. 4: 916–928.
Mora, E. A., S. T. Lindley, D. L. Erickson, and A. P. Klimley. 2009. “Do
Impassable Dams and Flow Regulation Constrain the Distribution
of Green Sturgeon in the Sacramento River, California?Journal of
Applied Ichthyology 25: 39 –47.
Morgan, R., M. H. Finnøen, H. Jensen, C. Pélabon, and F. Jutfelt. 2020.
“Low Potential for Evolutionary Rescue From Climate Change in a
Tropical Fish.” Proceedings of the National Academy of Sciences 117:
33365–33372.
Morley, S., L. Peck, J. Su nday, S. Heiser, and A. Bates. 2 019. “Physiological
Acclimation and Persistence of Ectothermic Species Under Extreme
Heat Events.” Global Ecology and Biogeography 28: 1018 –1037.
Moser, M. L., and S. T. Lindley. 2007. “Use of Washington Estuaries by
Subadult and Adult Green Sturgeon.” Environmental Biology of Fishes
79: 243–253.
Moyle, P. B., and R. A. Leidy. 1992. “Loss of Biodiversity in Aquatic
Ecosystems: Evidence From Fish Faunas.” In Conservation Biology:
The Theory and Practice of Nature Conser vation Preser vation and
Management, 127–169. Boston, MA: Springer.
Murren, C. J., J. R. Auld, H. Callahan, etal. 2015. “Constraints on the
Evolution of Phenotypic Plasticity: Limits and Costs of Phenotype and
Plasticity.” Heredity 115, no. 4: 293 –301.
Nakagawa, S., M. Lagisz, R. E. O’Dea, etal. 2023. “orchaRd 2.0: An R
Package for Visualizing Meta- Analyses With Orchard Plots.” Methods
in Ecology and Evolution 14, no. 8: 2003–2010.
Noble, D. W., P. Pottier, M. Lagis z, etal. 202 2. “Meta- Analytic Approaches
and Effe ct Sizes to Account for ‘Nuisa nce Heterogeneity in Comparative
Physiology.” Journal of Experimental Biology 225: jeb243225.
Paragamian, V. L., and G. Kruse. 2001. “Kootena i River White Sturgeon
Spawning Migration Behavior and a Predictive Model.” North Am erican
Journal of Fisheries Management 21, no. 1: 10–21.
Paragamian, V. L., and V. D. Wakkinen. 2011. “White Sturgeon
Spawning and Discharge Augmentation.” Fisheries Management and
Ecology 18, no. 4: 314–321.
Payne, N. L ., J. A. Smith, D. E. van der Meulen, etal. 2 016. “Temperat ure
Dependence of Fish Performance in the Wild: Links With Species
Biogeography and Physiological Thermal Tolerance.” Functional
Ecology 30: 903–912.
Penman, R. J., W. Bugg, B. Rost- Komiya, M. L. Earhart, and C. J.
Brauner. 2023. “Slow Heating Rates Increase Thermal Tolerance and
Alter mRNA HSP Expression in Juvenile White Sturgeon (Acipenser
transmontanus).” Journal of Thermal Biology 115: 103599.
Penny, F. M., W. S. Bugg, J. D. Kieffer, K. M. Jeffries, and S. A. Pavey.
2023. “Atlantic Sturgeon and Shortnose Sturgeon Exhibit Highly
Divergent Tran scriptomic Respons es to Acute Heat Stress .” Comparative
Biochemistry and Physiology Part D: Genomics and Proteomics 45:
101058.
Penny, F. M., and J. D. Kieffer. 2019. “Lack of Change in Swimming
Capacity (U Crit) Following Acute Salinity Exposure in Juvenile
Shortnose Sturgeon (Acipenser brevirostrum).” Fish Physiolog y and
Biochemistry 45: 1167–1175.
Perry, A. L., P. J. Low, J. R. Ellis, and J. D. Rey nolds. 2005. “Climate
Change and Distribution Shifts in Marine Fishes.” Science 308:
1912–1915.
Phelps, Q. E., S. J. T ripp, W. D. Hintz, etal. 2010. “Water Temperatu re and
River Stage Inf luence Mortality and Abundance of Naturally Occurring
Mississippi River Scaphirhynchus Sturgeon.” North Amer ican Journal of
Fisheries Management 30, no. 3: 767–775.
Pick, J. L., S. Nakagawa, and D. W. A. Noble. 2019. “Reproducible,
Flexible and High- Throughput Data Extraction From Primary
Literature: The Metadigitise R Package.” Methods in Ecology and
Evolution 10: 426 –431.
Poletto, J. B., B. Martin, E. Danner, etal. 2018. “Assessment of Multiple
Stressor s on the Growth of Lar val Green Sturgeon Ac ipenser Medirostris:
Implications for Recruitment of Early Life- History Stages.” Journal of
Fish Biology 93, no. 5: 952–960.
Pollock, M. S., M. Carr, N. M. Kreitals, and I. D. Phillips. 2015. “Review
of a Species in Peril: What We Do Not Know About Lake Sturgeon May
Kill Them.” Environmental Reviews 23, no. 1: 30–43.
Pottier, P., S. Burke, R. Y. Zhang, etal. 2022. “Developmental Plasticity
in Thermal Tolerance: Ontogenetic Variation, Persistence, and Future
Directions.Ecology Letters 25: 2245–2268.
Poytress, W. R., J. J. Gruber, J. P. Van Eenennaam, and M. Gard. 2015.
“Spatial and Temporal Distribution of Spawning Events and Habitat
Characteristics of Sacramento River Green Sturgeon.” Transactions of
the American Fisheries Society 144, no. 6: 1129–1142.
Raynal, R. S., D. W. Noble, J. L. Riley, etal. 2022. “Impact of Fluctuating
Developmental Temperatures on Phenotypic Traits in Reptiles: A Meta-
Analysis.” Journal of Experimental Biology 225: jeb243369.
Rodgers, E. M., J. B. Poletto, D. F. Gomez Isaza, etal. 2019. “Integrating
Physiological Data With the Conser vation and Management of Fishes:
A Meta- Analytical Review Using the Threatened Green Sturgeon
(Acipenser medirostris).” Conservation Physiology 7, no. 1: coz035.
Román- Palacios, C., and J. J. Wiens. 2020. “Recent Responses to
Climate Change Reveal the Drivers of Species Extinction and Survival.”
Proceedings of the National Academy of Sciences 117: 4211– 4217.
Ruthsatz, K., F. Dahlke, K. A lter, et al. 2024. “Acclimation Capacity
to Global Warming of Amphibians and Freshwater Fishes: Drivers,
Patterns, and Data Limitations.” Global Change Biology 30, no. 5:
e17318. https:// doi. org/ 10. 1111/ gcb. 17318 .
Sandblom, E., T. D. Clark, A. Gräns, et al. 2016. “Physiological
Constraints to Climate Warming in Fish Follow Principles of Plastic
Floors and Concrete Ceilings.” Nature Communications 7: 114 47.
Schreier, A. D., J. P. Van Eenennaam, P. Anders, S. Young, and J.
Crossman . 2021. “Sponta neous Autopolyploidy in the Acipens eriformes,
With Recommendations for Management.” Reviews in Fish Biology and
Fisheries 31, no. 2: 159–180. https:// doi. org/ 10. 1007/ s1116 0- 021- 09637 - z.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
19 of 24
Schulte, P. M. 2014. “What Is Environmental Stress? Insights From Fish
Living in a Variable Environment.” Journal of Ex perimental Biolog y 217,
no. 1: 23–34.
Schulte, P. M. 2015. “The E ffects of Temperatur e on Aerobic Metabolism:
Towards a Mechanistic Understanding of the Responses of Ectotherms
to a Changing Environment.” Journal of Experimental Biolog y 218:
1856–1866.
Schulte, P. M., T. M. Healy, and N. A. Fangue. 2011. “Thermal
Performance Curves, Phenotypic Plasticity, and the Time Scales of
Temperature Exposure.” Integrative and Comparative Biology 51, no. 5:
691–702.
Seebacher, F., C. R. White, and C. E. Franklin. 2015. “Physiological
Plasticity Increases Resilience of Ectothermic Animals to Climate
Change.” Nature Climate Change 5: 61–66.
Somero, G. 2010. “The Physiology of Climate Change: How Potentials
for Acclimatization and Genetic Adaptation Will Determine ‘Winners’
and ‘Losers’.” Journal of Experimental Biology 213: 912–920.
Spear, M. C., and J. D. Kieffer. 2016. “Critical Thermal Maxima and
Hematology for Juvenile Atlantic (Acipenser oxyrinchus Mitchill 1815)
and Shortnose (Acipenser brevirostrum Lesueur, 1818) Sturgeons.”
Journal of Applied Ichthyology 32, no. 2: 251–257.
Stillman, J. H. 2019. “Heat Waves, the New Normal: Summertime
Temperature Extremes Will Impact Animals, Ecosystems, and Human
Communities.” Physiology 34: 86 –100.
Sullivan, A. B., H. I. Jager, and R. Myers. 2003. “Modeling W hite
Sturgeon Movement in a Reservoir: The Effect of Water Quality and
Sturgeon Density.” Ecological Modelling 167, no. 1- 2: 97–114.
Sunday, J., J. M. Bennett, P. Calosi, et al. 2019. “Thermal Tolerance
Patterns Across Latitude and Elevation.” Philosophical Transactions of
the Royal Society B 374, no. 1778: 20190036.
Sunday, J. M., A. E. Bates, and N. K. Dulvy. 2011. “Global Analysis of
Thermal Tolerance and Latitude in Ectotherms.” Proceedings of the
Royal Society B: Biological Sciences 278, no. 1713: 1823–1830.
Sunday, J. M., A. E. Bates, and N. K. Dulvy. 2012. “Thermal Tolerance
and the Global Redistribution of Animals.” Nature Climate Change 2:
686–690.
Trifonov, V. A., S. S. Romanenko, V. R. Beklemisheva, et al. 2016.
“Evolutionary Plasticity of Acipenseriform Genomes.” Chromosoma
125: 661–668.
Van de Peer, Y., E. Mizrachi, and K. Marchal. 2017. “The Evolutionary
Significance of Polyploidy.” Nature Reviews Genetics 18: 411– 424.
Vasil'ev, V. P., E. D. Vasil’eva, S. V. Shedko, and G. V. Novomodny. 2010.
“How Many Times Has Polyploidization Occurred During Acipenserid
Evolution? New Data on the Karyotypes of Sturgeons (Acipenseridae,
Actinopterygii) From the Russian Far East.” Journal of Ichthyology 50:
950–959.
Vasseur, D. A., J. P. DeLong, B. Gilbert, et al. 2014. “Increased
Temperature Variation Poses a Greater Risk to Species Than Climate
Warmi ng .” Proceedings of the Royal Society B: Biological Sciences 281:
20132612 .
Verhille, C. E., J. B. Poletto, D. E. Cocherell, etal. 2014. “Larval Green
and White Sturgeon Sw imming Performance in Relation to Water-
Diversion Flows.” Conservation Physiology 2, no. 1: cou031.
Viechtbauer, W. 2010. “Conducting Meta- Analyses in R With the Meta-
For Package.” Journal of Statistical Soft ware 36: 1–48.
Weber, T. A., A. M. Dichiera, and C. J. Brauner. 2024. “Resetting
Thermal Limits: 10- Year- Old White Sturgeon Display Pronounced but
Reversible Thermal Plasticity.” Journal of Thermal Biology 103 807.
Wikelski, M., and S. J. Cooke. 2006. “Conservation Physiology.” Trends
in Ecology & Evolution 21: 38–46.
Zhang, Y., and J. D. Kieffer. 2014. “Critica l Thermal Maxi mum (CTmax)
and Hematology of Shortnose Sturgeons (Acipenser brevirostrum)
Acclimated to Three Temperatures.” Canadian Journal of Zoology 92,
no. 3: 215–221.
Ziegeweid, J. R., C. A. Jennings, D. L. Peterson, and M. C. Black. 2008.
“Effects of Salinity, Temperature, and Weight on the Survival of Young-
Of- Year Shortnose Sturgeon.” Transactions of the American Fisheries
Society 137, no. 5: 1490–1499.
Data Sources
Adams, S. R., G. L. Adams, and G. R. Parsons. 20 03. “Critical
Swimming Speed and Behavior of Juvenile Shovelnose Sturgeon and
Pallid Sturgeon.” Trans actions of the Amer ican Fisher ies Society 132 , no.
2: 392–397.
Allen, P. J., B. Hodge, I. Werner, and J. J. Cech Jr. 2006. “Effects of
Ontogeny, Season, and Temperature on the Swimming Performance of
Juvenile Green Sturgeon (Acipenser medirostris).” Canadian Journal of
Fisheries and Aquatic Sciences 63, no. 6: 1360–1369.
Allen, P. J., M. Nicholl, S. Cole, A. Vlazny, and J. J. Cech Jr. 2006.
“Growth of Larval to Juvenile Green Sturgeon in Elevated Temperature
Reg imes.” Transactions of the American Fisheries Society 135, no. 1:
89–96.
Aloisi, D. B., O. T. Eckes, and A. J. Von Eschen. 2019. “Development
of a Growth Model for Lake Sturgeon.” North American Journal of
Aquaculture 81, no. 4: 399–405.
Auer, N. A. 1996. “Response of Spawning Lake Sturgeons to Change
in Hydroelectric Facility Operation.” Transactions of the American
Fisheries Society 125, no. 1: 66–77.
Auer, N. A., and E. A. Baker. 2002. “Duration and Drift of Larval
Lake Sturgeon in the Sturgeon River, Michigan.” Journal of Applied
Ichthyology 18.
Bain, M., N. Haley, D. Peterson, J. R. Waldman, and K. A rend. 2000.
“Har vest and Habitats of Atla ntic Sturgeon Acipenser ox yrinchus Mitchill,
1815 in the Hudson River Estuary: Lessons for Sturgeon Conservation.”
Boletin- Instituto Espanol De Oceanografia 16, no. 1/4: 43–54.
Baker, D. W., D. S. O. McAdam, M. Boucher, K. T. Huynh, and C. J.
Brauner. 2014. “Sw imming Perfor mance and Larva l Quality are A ltered
by Rearing Substrate at Early Life Phases in White Sturgeon, Acipenser
transmontanus (Richardson, 1836).” Journal of Applied Ichthyolog y 30,
no. 6: 1461–1472.
Bard, B., and J. D. Kieffer. 2019. “The Effects of Repeat Acute Thermal
Stress on the Critical Thermal Maximum (CTmax) and Physiology of
Juvenile Shortnose Sturgeon (Acipenser brevirostrum).” Canadian
Journal of Zoology 97, no. 6: 567–572.
Baril, A. M., J. T. Buszkiewicz, P. M. Biron, Q. E. Phelps, and J. W. A.
Grant. 2018. “Lake Sturgeon (Acipenser fulvescens) Spawning Habitat:
A Quantitative Review.” Canadian Journal of Fisheries and Aquatic
Sciences 75: 925–933.
Bates, L. C., M. A. Boucher, and J. M. Shrimpton. 2014. “Effect of
Temperature and Substrate on Whole Body Cortisol and Size of Lar val
White Sturgeon (Acipenser transmontanus Richardson, 1836).” Journal
of Applied Ichthyology 30, no. 6: 1259–1263.
Beardsall, J. W., M. J. W. Stokesbury, L. M. Logan- Chesney, and M. J.
Dadswell. 2016. “Atlantic Sturgeon Acipenser oxyrinchus Mitchill, 1815
Seasonal Marine Depth and Temperature Occupancy and Movement in
the Bay of Fundy.” Journal of Applied Ichthyology 32, no. 5: 809–819.
Boothroyd, M. L., T. J. Haxton, C. Hendry, D. A. Romain, C. C.
Wilson, and T. Whillans. 2019. “Post- release Dispersal and Spawning
Movements of a Translocated Lake Sturgeon (Acipenser fulvescens,
Rafinesque 1817) Population in the Mattagami River, Ontario.” Journal
of Applied Ichthyology 35, no. 1: 103–116.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
20 of 24 Global Change Biology, 2024
Borodin, N. 1925. “Biological Observations on the Atlantic Sturgeon
(Acipenser sturio).” Transactions of the American Fisheries Society 55,
no. 1: 184–190.
Boucher, M. A., S. O. McAdam, and J. M. Shrimpton. 2014. “The
Effect of Temperature and Substrate on the Growth, Development and
Survival of Larval White Sturgeon.” Aquaculture 430: 139 –148.
Breece, M. W., D. A. Fox, K. J. Dunton, M. G. Frisk, A. Jordaan, and M.
J. Oliver. 2016. “Dynamic Seascapes Predict the Marine Occurrence of
an Endangered Species: Atlantic Sturgeon Acipenser oxyrinchus ox yrin-
chus.” Methods in Ecology and Evolution 7, no. 6: 725–733.
Breece, M. W., D. A. Fox, D. E. Haulsee, I. I. Wirgin, and M. J. Oliver.
2018. “Satellite Driven Distribution Models of Endangered Atlantic
Sturgeon Occurrence in the Mid- Atlantic Bight.” ICES Journal of
Marine Science 75, no. 2: 562–571.
Breece, M. W., D. A. Fox, a nd M. J. Oliver. 2018. “Environmenta l Drivers
of Adult Atlantic Sturgeon Movement and Residency in the Delaware
Bay.” Marine and Coastal Fisheries 10, no. 2: 269–280.
Brown, K. 2007. “Evidence of Spawning by Green Sturgeon, Acipenser
medirostris, in the Upper Sacramento River, California.” Environmental
Biology of Fishes 79: 297–303.
Bruch, R. M., and F. P. Binkowski. 2002. “Spawning Behavior of Lake
Sturgeon (Acipenser fulvescens).” Journal of Applied Ichthyology 18:
570–579.
Bugg, W. S., G. R. Yoon, C. Br andt, M. L. Earha rt, W. G. Anderson, and K.
M. Jeffries. 2021. “ The Effects of Population and Thermal Acclimation
on the Growth, Condition and Cold Responsive Mrna Expression of
Age- 0 Lake Sturgeon (Acipenser fulvescens).” Journal of Fish Biology 99,
no. 6: 1912–1927.
Bugg, W. S., G. R. Yoon, A. N . Schoen, etal. 20 20. “Effect s of Acclimation
Temperature on the T hermal Physiology in Two Geogr aphically Distinct
Populations of Lake Sturgeon (Acipenser fulvescens).” Conser vation
Physiology 8: coaa087.
Bugg, W. S., G. R. Yoon, A. N. Schoen, A. M. Weinrauch, K. M. Jeffries,
and W. G. Anderson. 2023. “Elevated Temperatures Dampen the Innate
Immune Capacity of Developing Lake Sturgeon (Acipenser fulvescens).”
Journal of Experimental Biology 226: jeb245335.
Caron, F., D. Hatin, and R. Fortin. 2002. “Biological Characteristics
of Adult Atlantic Sturgeon in the St Lawrence River Estuary and the
Effectiveness of Management Rules.” Journal of Applied Ichthyology 18,
no. 4–6: 580–585.
Carr, S. H., F. Tatman, and F. A. Chapman. 1996. “Obser vations on the
Natural History of the Gulf of Mexico Sturgeon (Acipenser oxyrinchus
de sotoi Vladykov 1955) in the Suwannee River, Southeastern United
State s.” Ecology of Freshwater Fish 5, no. 4: 169–174.
Caswell, N. M., D. L. Peterson, B. A. Manny, and G. W. Kennedy. 2004.
“Spawning by Lake Sturgeon (Acipenser fulvescens) in the Detroit
River.” Journal of Applied Ichthyology 20, no. 1: 1–6.
Cech, J. J., S. J. Mitchell, and T. E. Wragg. 1984. “Comparative Growth
of Juvenile White Sturgeon and Striped Bass: Effects of Temperature
and Hypoxia.” Estuaries 7: 12–18.
Chapman, C. G., and T. A. Jones. 2010. “First Documented Spawning
of White Sturgeon in the Lower Willamette River, Oregon.” Northwest
Science 84, no. 4: 327–335.
Chapman, F. A., and S. H. Carr. 1995. “Implications of Early Life Stages
in the Natural History of the Gulf of Mexico Sturgeon, Acipenser oxyr in-
chus de sotoi.” Environmental Biology of Fishes 43: 407–413.
Chiotti, J. A., J. M. Holtgren, N. A. Auer, and S. A. Ogren. 2008. “Lake
Sturgeon Spaw ning Habitat in the Big Manistee River, Michigan.”
North American Journal of Fisheries Management 28, no. 4: 1009–1019.
Chipps, S. R ., R. A. Klumb, and E. B. Wright. 2010. “Development and
Application of Juvenile Pallid Sturgeon Bioenergetics Model.” Final
report to South Dakota Department of Game, Fish and Parks, Federal
Aid Project Number T- 24- R, 2424.
Collins, M. R., T. I. Smith, W. C. Post, and O. Pashuk. 2000. “Habitat
Utilization and Biological Characteristics of Adult Atlantic Sturgeon
in Two South Carolina R ivers.” Transactions of the American Fisheries
Society 129, no. 4: 982–988.
Collins, M. R., W. C. Post, and D. C. Russ. 20 01. “Distribution of
Shortnose Sturgeon in the Lower Savannah River.” Final Report to the
Georgia Ports Authority.
Cooke, D. W., and S. D. Leach. 2004. “Implications of a Migration
Impediment on Shortnose Sturgeon Spawning.” North American
Journal of Fisheries Management 2 4, no. 4: 1460 1468.
Dadswell, M. J. 1979. “Biology and Population Characteristics of the
Shortnos e Sturgeon , Acipenser brevirost rum LeSue ur 1818 (Osteichthyes:
Acipenseridae), in the Saint John River Estuar y, New Brunswick,
Canada.” Canadian Journal of Zoology 57, no. 11: 2186–2210.
Dammerman, K. J., M. A. Webb, and K. T. Scribner. 2019. “Riverine
Charact eristics and Adult Demogr aphy Influence Female L ake Sturgeon
(Acipenser fulvescens) Spawning Behavior, Reproductive Success, and
Ovarian Quality.” Canadian Journal of Fisheries and Aquatic Sciences
76, no. 7: 1147–1160.
Dammerman, K. J., J. P. Steibel, and K. T. Scribner. 2016. “Increases
in the Mean and Variability of Thermal Regimes Result in Differential
Phenotypic Responses Among Genotypes During Early Ontogenetic
Stages of Lake Sturgeon (Acipenser fulvescens).” Evolutionary
Applications 9, no. 10: 1258–1270.
Damstra, R. A., and T. L. Galarowicz. 2013. “Summer Habitat Use
by Lake Sturgeon in Manistee Lake, Michigan.” Transactions of the
American Fisheries Society 142, no. 4: 931–941.
DeLonay, A. J., K. A. Chojnacki, R. B. Jacobson, etal. 2016. “Ecological
Requirements for Pallid Sturgeon Reproduction and Recruitment in the
Missouri River—A Synthesis of Science, 2005 to 2012 (No. 2015- 5145).”
US Geological Survey.
Deslauriers, D., and J. D. Kieffer. 2012. “T he Effects of Temperature on
Swimming Performance of Juvenile Shortnose Sturgeon (Acipenser bre-
virostrum).” Journal of Applied Ichthyology 28, no. 2: 176–181.
DeVries, R. J. 2006. “Population Dynamics, Movements, and Spawning
Habitat of the Shortnose Sturgeon, Acipenser brevirostrum, in the
Altamaha River system, Georgia.” Doctoral Dissertation, University of
Georgia.
Dumont, P., J. D’Amours, S. Thibodeau, et al. 2011. “Effects of the
Development of a Newly Created Spawning Ground in the Des
Prairies River (Quebec, Canada) on the Reproductive Success of Lake
Sturgeon (Acipenser fulvescens).” Journal of Applied Ichthyolog y 27, no.
2: 394–404.
Duncan, M. S., J. J. Isely, and D. W. Cooke. 2004. “Evaluation of
Shortnose Sturgeon Spawning in the Pinopolis Dam Tailrace, South
Carolina.North American Journal of Fisheries Management 24, no. 3:
932–938.
Dunton, K. J., A . Jordaan, K. A . McKown, D. O. Conover, and M. G. Fr isk.
2010. “Abundance and Distr ibution of Atlantic St urgeon (Acipenser oxy-
rinchus) Within the Northwest Atlantic Ocean, Determined from Five
Fishery- Independent Surveys.” Fisher y Bulletin 108: 450 –465.
Duong, T. Y., K. T. Scribner, J. A. Crossman, P. S. Forsythe, and E. A.
Baker. 2011. “Environmental and Maternal Effects on Embryonic and
Lar val Developmental Time Until D ispersal of Lake Stu rgeon (Acipenser
fulvescens).” Canadian Journal of Fisheries and Aquatic Sciences 68, no.
4: 643–654.
Earhar t, M. L., T. S. Bla nchard, P. R. Morrison, etal. 2023a . “Identification
of Upper Thermal Thresholds During Development in the Endangered
Nechako White Sturgeon with Management Implications for a
Regulated River.” Conservation Physiology 11: coad032.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
21 of 24
Earhart, M. L., T. S. Blanchard, N. Strowbridge, etal. 2023b. “Heatwave
Resilience of Juvenile White Sturgeon is Associated With Epigenetic
and Transcriptional Alterations.” Scientific Reports 13: 15451.
Ecclestone, A., T. J. Haxton, T. C. Pratt, C. C. Wilson, and T. Whillans.
2020. “Seasonal use of Two Unregulated Lake Superior Tributaries by
Lake Sturgeon.” Journal of Great Lakes Research 46, no. 5: 1369–1381.
Ecclestone, A. 2012. “Movement Patterns, Habitat Utilization, and
Spawning Habitat of Lake Sturgeon (Acipenser fulvenscens) in the Pic
River, a Northeastern Lake Superior Tributary in Ontario, Canada.”
Master's Thesis, Trent University.
Edwards, R. E., K. J. Sulak, M. T. Randall, and C. B. Grimes. 2003.
“Movements of Gulf Sturgeon (Acipenser oxyrinchus desotoi) in
Nearshore Habitat as Determined by Acoustic Telemetry.” Gulf of
Mexico Science 21, no. 1: 5.
Elliott, C. M., A. J. DeLonay, K. A. Chojnacki, and R. B. Jacobson. 2020.
“Characterization of Pallid Sturgeon (Scaphirhynchus albus) Spawning
Habitat in the Lower Missour i River.” Journal of Applied Ichthyol ogy 36,
no. 1: 25–38.
Erickson, D. L., A. Kahnle, M. J. Millard, et al. 2011. “Use of Pop- up
Satellite A rchival Tags to Identif y Oceanic- Migratory Patterns for Adult
Atlantic Sturgeon, Acipenser oxyrinchus oxyrinchus Mitchell, 1815.”
Journal of Applied Ichthyology 27, no. 2: 356–365.
Erickson, D. L ., and M. A. Webb. 2007. “Spaw ning Periodicity, Spaw ning
Migration, and Size at Maturity of Green Sturgeon, Acipenser mediros-
tris, in the Rogue River, Oregon.” Environmental Biology of Fishes 79:
255–2 68.
Erickson, D. L., J. A. North, J. E. Hightower, J. Weber, and L. Lauck.
2002. “Movement and Habitat Use of Green Sturgeon Acipenser med-
irostris in the Rogue R iver, Oregon, USA.” Journal of A pplied Ichthyolog y
18, no. 4- 6: 565–569.
Forsythe , P. S., K. T. Scribner, J. A . Crossman, etal. 2012. “E nvironmental
and Lunar Cues are Predictive of the Timing of River Entry and
Spawning- Site Arrival in Lake Sturgeon Acipenser fulvescens.” Journal
of Fish Biology 81, no. 1: 35–53.
Foster, A. M., and J. P. Clugston. 1997. “Seasonal Migration of Gulf
Sturgeon in the Suwanne e River, Florida.” Transac tions of the Ameri can
Fisheries Society 126, no. 2: 302–308.
Fox, D. A., J. E. Hightower, and F. M. Parauka. 200 0. “Gulf Sturgeon
Spawning Migration and Habitat in the Choctawhatchee River System,
Alabama–Florida.” Transactions of the American Fisheries Society 129,
no. 3: 811–826.
Fuller, D. B., M. E . Jaeger, and M. Webb. 2008. “ Spawning a nd Associated
Movement Patterns of Pallid Sturgeon in the Lwer Yellowstone River.”
Upper Basin Pallid Sturgeon Recover y Workgroup 2007 Annual Report.
Upper Basin Workgroup, US Fish and Wildlife Service, Bozeman.
Geist, D. R., R. S. Brown, V. Cullinan, et al. 2005. “Movement,
Swimming Speed, and Oxygen Consumption of Juvenile White
Sturgeon in Response to Changing Flow, Water Temperature, and Light
Lvel in the Snake River, Idaho.” Transactions of the American Fisheries
Society 134, no. 4: 803–816.
Goodma n, B. J., C. S. Guy, S. L. C amp, W. M. Gardner, K. M . Kappenman,
and M. A. H. Webb. 2013. “Shovelnose Sturgeon Spawning in Relation
to Varying Discharge Treatments in a Missouri River Tributary.” River
Research and Applications 29, no. 8: 1004–1015.
Gradil, A. M., G. M. Wright, D. J. Speare, D. W. Wadowska, S. Purcell,
and M. D. Fast. 2014. “The Effects of Temperature and Body size on
Immunologica l Development and Responsiveness in Juveni le Shortnose
Sturge on (Acipenser brevirostrum).” Fish & Shellf ish Immunology 4 0, no.
2: 545 –555.
Gutreuter, S., J. M. Vallazza, and B. C. K nights. 2010. “Lateral
Distribution of Fishes in the Main- Channel Trough of a Large
Floodplain R iver: Implications for Restoration.” River Research and
Applications 26, no. 5: 619–635.
Hager, C. H., J. C. Watter son, and J. E. Kah n. 2020. “S pawning Driv ers and
Frequency of Endangered Atlantic Sturgeon in the York River System.”
Transactions of the American Fisheries Society 149, no. 4: 474–485.
Hall, J. W., T. I. Smith, and S. D. Lamprecht. 1991. “Movements and
Habitats of Short nose Sturgeon, Acipenser bre virostrum in the Sava nnah
River.” Copeia: 695 –702.
Hardy, R. S., and M. K. Litvak. 20 04. “Effects of Temperature on the
Early Development, Growth, and Survival of Shortnose Sturgeon,
Acipenser brevirostrum, and Atlantic Sturgeon, Acipenser ox yrhynchus,
Yolk- Sac Larvae.” Environmental Biolog y of Fishes 70: 145–154.
Harkness, W. J. K., and J. R. Dymond. 1961. The Lake Sturgeon: The
History of its Fishery and Problems of Conser vation, 121. Toronto:
Ontario Department of Lands and Forests, Fish and Wildlife Branch.
Harris, J. E., D. C. Pa rkyn, and D. J. Murie. 20 05. “Distribution of Gulf of
Mexico Stu rgeon in Relation to Benthic Inver tebrate Prey Resource s and
Environmental Parameters in the Suwannee River Estuar y, Florida.”
Transactions of the American Fisheries Society 134, no. 4: 975–990.
Hatin, D., R. Fortin, and F. Caron. 2002. “Movements and Aggregation
Areas of Adult Atlantic Sturgeon (Acipenser oxyrinchus) in the
St Lawrence R iver Estuary, Quebec, Canada.” Journal of Applied
Ichthyology 18, no. 4- 6: 586–594.
Heise, R. J., W. T. Slack, S. T. Ross, a nd M. A. Dugo. 2005 . “Gulf Sturgeon
Summer Habitat Use and Fall Migration in the Pascagoula River,
Mississippi, USA.” Journal of Applied Ichthyology 21, no. 6: 461–468.
Hightower, J. E., K. P. Zehfuss, D. A. Fox, and F. M. Parauka. 2002.
“Summer Habitat Use by Gulf Sturgeon in the Choctawhatchee R iver,
Florida .” Journal of Applied Ichthyology 18. https:// doi. org/ 10. 1046/j.
1439- 0426. 2002. 00402. x.
Huff, D. D., S. T. Lindley, P. S. Rankin, and E. A. Mora. 2011. “Green
Sturgeon Physical Habitat use in the Coastal Pacif ic Ocean.” PLoS One
6, no. 9: e25156.
Huff, D. D., S. T. Lindley, B. K. Wells, and F. Chai. 2012. “Green
Sturgeon Distribution in the Pacific Ocean Estimated from Modeled
Oceanographic Features and Migration Behavior.” PLoS One 7, no. 9:
e45852.
Hung, S. S., P. B. Lutes, A. A. Shqueir, and F. S. Conte. 1993. “Effect
of Feeding Rate and Water Temperature on Growth of Juvenile White
Sturgeon (Acipenser transmontanus).” Aquaculture 115, no. 3- 4:
297–3 03.
Hurley, K. L., R. J. Sheehan, R. C. Heidinger, P. S. Wills, and B.
Clevenstine. 2004. “Habitat use by Middle Mississippi River Pallid
Sturgeon.” Transactions of the American Fisheries Societ y 133, no. 4:
1033–1041.
Ingram, E. C., and D. L. Peterson. 2016. “Annual Spawning Migrations
of Adult Atlantic Sturgeon in the A ltamaha River, Georg ia.” Marine and
Coastal Fisheries 8, no. 1: 595–606.
Ingram, E. C., and D. L. Peterson. 2018. “Seasonal Movements of
Shortnose Sturgeon (Acipenser brevirostrum) in the Altamaha R iver,
Georgia.” River Research and Applications 34, no. 7: 873–882.
Ingram, E. C., R. M. Cerrato, K. J. Dunton, and M. G. Frisk. 2019.
“Endangered Atlantic Sturgeon in the New York Wind Energy Area:
Implications of Future Development in an Offshore Wind Energy Site.”
Scientific Reports 9, no. 1: 12432.
Izzo, L. K., D. L. Parrish, and G. B. Zydlewski. 2021. “Multi- Run
Migrator y Behavior of Adult Male Lake Sturgeon in a Short River.”
Journal of Great Lakes Research 47, no. 5: 1400–1409.
Jackson, Z. J., J. J. Gruber, and J. P. Van Eenennaam. 2016. “White
Sturgeon Spaw ning in the San Joaquin River, California, and Effects
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
22 of 24 Global Change Biology, 2024
of Water Management.” Journal of Fish and Wildlife Management 7, no.
1: 17 1–180.
Johnson, J. H., S. R. LaPan, R. M. Klindt, and A. Schiavone. 2 006. “Lake
Sturgeon Spaw ning on Artificial Habitat in the St Lawrence River.”
Journal of Applied Ichthyology 22, no. 6: 465– 470.
Kappenman, K. M., M. A. H. Webb, and M. Greenwood. 2013. “The
Effect of Temperature on Embryo Surv ival and Development in Pallid
Sturgeon Scaphirhynchus albus (Forbes & Richardson 1905) and
Shovelnose Sturgeon S. Platorynchus (Rafinesque, 1820).” Journal of
Applied Ichthyology 29, no. 6: 1193–1203.
Kelly, J. L., and D. E. Arnold. 1999. “Effects of Ration and Temperature
on Growth of Age- 0 Atlantic Sturgeon.” North American Journal of
Aquaculture 61, no. 1: 51–57.
Kelly, J. T., A. P. Klimley, and C. E. Crocker. 20 07. “Movements of Green
Sturgeon, Acipenser medirostris, in the San Francisco Bay Estuar y,
California.” Environmental Biolog y of Fishes 79: 281–295.
Kennedy, A. J., T. M. Sutton, and B. E. Fisher. 2006. “Reproductive
Biology of Female Shovelnose Sturgeon in the Upper Wabash River,
Ind iana .” Journal of Applied Ichthyology 22, no. 3: 177–182.
Kieffer, J. D., F. M. Penny, and V. Papadopoulos. 2014. “Temperature
has a Reduced Effect on Routine Metabolic Rates of Juvenile Shortnose
Sturgeon (Acipenser brevirostrum).” Fish Physiology and Biochemistry
40: 551–559.
Kieffer, M. C., and B. Kynard. 1993. “Annual Movements of Shortnose
and Atlantic Sturgeons in the Merrimack River, Massachusetts.”
Transactions of the American Fisheries Society 122, no. 6: 1088–1103.
Kieffer, J. D., and B. Bard. 2022. “Critical Thermal Maximum and
Minimum of Juvenile Shortnose Sturgeon (Acipenser brevirostrum)
Acclimated to 12 and 18°C.” Journal of Applied Ichthyology 38, no. 5:
526–530.
Kieffer, M. C., and B. Kynard. 1996. “Spawning of the Shortnose
Sturgeon in the Merrimack River, Massachusetts.” Transactions of the
American Fisheries Society 125, no. 2: 179–186.
Killgore, K. J., J. J. Hoover, S. G. George, B. R. Lewis, C. E. Murphy,
and W. E. Lancaster. 2007. “Distribution, Relative Abundance and
Movements of Pallid Sturgeon in the Free- Flowing Mississippi River.”
Journal of Applied Ichthyology 23, no. 4: 476–483.
Kolman, R., O. Khudyi, O. Kushniryk, L. Khuda, M. Prusinska, and G.
Wiszniewski. 2018. “Influence of Temperature and Artemia Enriched
with ω- 3 PUFA s on the Early Ontogene sis of Atlantic Sturgeon, Acipenser
oxyrinchus Mitchill, 1815.” Aquaculture Research 49, no. 5: 1740–1751.
LaHaye, M ., A. Branchaud, M. Gendron, R . Verdon, and R. Fortin. 1992.
“Reproduction, Early Life History, and Characteristics of the Spawning
Grounds of the Lake Sturgeon (Acipen ser fulvescens) in Des Prairies and
L'Assomption Rivers, Near Montreal, Quebec.” Canadian Journal of
Zoology 70, no. 9: 1681–1689.
Lallaman, J. J., R. A. Damstra, and T. L. Galarowicz. 2008. “Population
Assessment and Movement Patterns of Lake Sturgeon (Acipenser ful-
vescens) in the Manistee River, Michigan, USA.” Journal of Applied
Ichthyology 24, no. 1: 1–6.
Lee, S., S. S. Hung, N. A . Fangue, etal. 2016. “Effects of Feed Restriction
on the Upper Temperature Tolerance and Heat Shock Response in
Juvenile Green and White Sturgeon.” Comparative Biochemistry and
Physiolog y Part A: Molecular & Integrative Physiology 198: 87–95.
Linare s- Casenave, J., I. Werner, J. P. Van Eenennaam, and S . I. Doroshov.
2013. “Temperature Stress Induces Notochord Abnormalities and Heat
Shock Proteins Expression in Larval Green Sturgeon (Acipenser med-
irostris Ayres 1854).” Journal of Applied Ichthyolog y 29, no. 5: 958–967.
Lutes, P. B., S. S. Hung, and F. S. Conte. 1990. “Survival, Growth,
and Body Composition of White Sturgeon Lar vae fed Purified and
Commercial Diets at 14.7 and 18.4°C.” Progressive Fish- Culturist 52, no.
3: 192–196.
Lyons, J., D. Walchak, J. Haglund, P. Kanehl, and B. Pracheil. 2016.
“Habitat use and Population Characteristics of Potentially Spawning
Shovelnose Sturgeon Scaphirhynchus plator ynchus (Rafinesque, 1820),
Blue Sucker (Cycleptus elongatus (Lesueur, 1817)), and Associated
Species in the Lower Wisconsin River, USA.” Journal of Applied
Ichthyology 32, no. 6: 1003–1015.
Marchant, S. R., and M. K. Shutters. 1996. “Artificial Substrates Collect
Gulf Sturgeon Eggs.” North American Journal of Fisheries Management
16, no. 2: 445–447.
Mayfield, R. B., and J. J. Cech Jr. 2004. “Temperature Effects on Green
Sturgeon Bioenergetics.” Transactions of the American Fisheries Societ y
133, no. 4: 961–970.
McCabe, G. T., Jr., and C. A. Tracy. 1994. “Spawning and Early Life
History of White Sturgeon, Acipenser transmontanus, in the Lower
Columbia River.” Fishery Bulletin 92, no. 4: 760–772.
McDonald, L., and T. Haxton. 2023. “Spatiotemporal use of a Tributar y
by Lake Sturgeon Over a 10- year Period.” Environmental Biology of
Fishes 106, no. 5: 853–874.
McKinley, S., G. Van Der Kraak, and G. Power. 1998. “Seasonal
Migrations and Reproductive Patterns in the Lake Sturgeon, Acipenser
fulvescens, in the Vicinity of Hydroelectric Stations in Northern
Ontario.” Environmental Biology of Fishes 51: 45–256.
Moore, M. J., C. P. Paukert, B. L . Brooke, and T. L. Moore. 2022. “Lake
Sturgeon Seasonal Movements in Regulated and Unregulated Missouri
River Tributaries.” Ecohydrology 15, no. 1: e2362.
Mora, E. A., S. T. Lindley, D. L. Erickson, and A. P. Klimley. 2009. “Do
Impassable Dams and Flow Regulation Constrain the Distribution
of Green Sturgeon in the Sacramento River, California?Journal of
Applied Ichthyology 25: 39 –47.
Moser, M. L., and S. T. Lindley. 2007. “Use of Washington Estuaries by
Subadult and Adult Green Sturgeon.” Environmental Biology of Fishes
79: 243–253.
Moser, M. L., and S. W. Ross. 1995. “Habitat Use and Movements of
Shortnose and Atlantic Sturgeons in the Lower Cape Fear River, North
Carolina. Transactions of the American Fisheries Society 124, no. 2:
225–234.
North, J. A., R. C. Beamesderfer, and T. A. Rien. 1993. “Distribution
and Movements of White Sturgeon in Three Lower Columbia River
Reser voir s.” Northwest Science 67, no. 2.
Odenkirk, J. S. 1989. “Movements of Gulf of Mexico Sturgeon in the
Apalachicola R iver, Florida.” Proceedings of the Annual Conference of
the Southeastern Association of Fish and Wildlife Agencies 43: 230–238.
Paragamian, V. L., and G. Kruse. 2001. “Kootena i River White Sturgeon
Spawning Migration Behavior and a Predictive Model.” North Am erican
Journal of Fisheries Management 21, no. 1: 10–21.
Paraga mian, V. L., G. Kruse , and V. Wakkinen. 20 01. “Spawnin g Habitat
of Kootenai River White Sturgeon, Post- Libby Dam.” North American
Journal of Fisheries Management 21, no. 1: 22–33.
Paraga mian, V. L., and V. D. Wakkinen. 2 002. “Tempora l Distribution of
Kootenai R iver White Sturgeon Spaw ning Events and the Ef fect of Flow
and Temperature.” Journal of Applied Ichthyology 18, no. 4- 6: 542–549.
Paragamian, V. L., and V. D. Wakkinen. 2011. “White Sturgeon
Spawning and Discharge Augmentation.” Fisheries Management and
Ecology 18, no. 4: 314–321.
Parauka, F. M., S. K. Alam, and D. A. Fox. 2001. “Movement and
Habitat use of Subadu lt Gulf Stu rgeon in Choctawhatchee Bay, Flor ida.”
Proceedings of the Annual Conference of the Southeastern Association of
Fish and Wildlife Agencies 55: 2 80–297.
Parsley, M. J., and L . G. Beckman. 1994. “White St urgeon Spawning a nd
Rearing Habitat in the Lower Columbia River.” North American Jour nal
of Fisheries Management 14, no. 4: 812–827.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
23 of 24
Parsley, M. J., L. G. Beckman, and G. T. McCabe Jr. 1993. “Spawning
and Rearing Habitat Use by W hite Sturgeons in the Columbia R iver
Downstream from McNary Dam.” Transactions of the Amer ican
Fisheries Society 122, no. 2: 217–227.
Penman, R. J., W. Bugg, B. Rost- Komiya, M. L. Earhart, and C. J.
Brauner. 2023. “Slow Heating Rates Increase Thermal Tolerance and
Alter mRNA HSP Expression in Juvenile White Sturgeon (Acipenser
transmontanus).” Journal of Thermal Biology 115: 103599.
Penman, R. 2021. The Effects of Temperature Acclimation and
Heating Rate on the Thermal Tolerance of Juvenile White Sturgeon
(Acipenser transmontanus) Master's Thesis, University of British
Columbia.
Penny, F. M., W. S. Bugg, J. D. Kieffer, K. M. Jeffries, and S. A. Pavey.
2023. “Atlantic Sturgeon and Shortnose Sturgeon Exhibit Highly
Divergent Tran scriptomic Respons es to Acute Heat Stress .” Comparative
Biochemistry and Physiology Part D: Genomics and Proteomics 45:
101058.
Perrin, C. J., L. L. Rempel, and M. L. Rosenau. 20 03. “White Sturgeon
Spawning Habitat in an Unregulated River: Fraser River, Canada.”
Transactions of the American Fisheries Society 132, no. 1: 154–165.
Phelps, Q. E., S. J. T ripp, W. D. Hintz, etal. 2010. “Water Temperatu re and
River Stage Inf luence Mortality and Abundance of Naturally Occurring
Mississippi River Scaphirhynchus Sturgeon.” North Amer ican Journal of
Fisheries Management 30, no. 3: 767–775.
Poletto, J. B., B. Martin, E. Danner, etal. 2018. “Assessment of Multiple
Stressors on the Growth of Larval Green Sturgeon Acipenser mediros-
tris: Implications for Recruitment of Early Life- History Stages.” Journal
of Fish Biology 93, no. 5: 952–960.
Poytress, W. R., J. J. Gruber, J. P. Van Eenennaam, and M. Gard. 2015.
“Spatial and Temporal Distribution of Spawning Events and Habitat
Characteristics of Sacramento River Green Sturgeon.” Transactions of
the American Fisheries Society 144, no. 6: 1129–1142.
Rodgers, E. M., A. E. Todgham, R. E. Connon, and N. A. Fangue.
2019. “Stressor Interactions in Freshwater Habitats: Effects of Cold
Water Exposure and Food Limitation on Early- Life Growth and Upper
Thermal Tolerance in White Sturgeon, Acipenser transmontanus.”
Freshwater Biology 64, no. 2: 348–358.
Rothermel, E. R., M. T. Balazik, J. E. Best, et al. 2020. “Comparative
Migration Ecology of Striped Bass and Atlantic Sturgeon in the US
Southern Mid- Atlantic Bight Fly way.PLoS One 15, no. 6: e02344 42.
Roussow, G. 1957. “Some Considerations Concerning Sturgeon
Spawning Periodicity.” Journal of the Fisheries Board of Canada 14, no.
4: 553–572.
Rusak, J. A., and T. Mosindy. 1997. “Seasonal Movements of Lake
Sturgeon in Lake of the Woods and the R ainy River, Ontario.” Canadian
Journal of Zoology 75, no. 3: 383–395.
Sardella, B. A., E. Sanmarti, and D. Kültz. 2008. “The Acute
Temperature Tolerance of Green Sturgeon (Acipenser medirostris) and
the Effect of Environmental Salinity.” Journal of Experimental Zoology
Part A: Ecological Genetics and Physiolog y 309, no. 8: 477–483.
Secor, D. H., M. H. P. O’Brien, N. C oleman, etal. 20 22. “Atlantic Sturgeon
Status and Mov ement Ecology i n an Extremely Smal l Spawning Habitat:
The Nanticoke River- Marshyhope Creek, Chesapeake Bay.” Reviews in
Fisheries Science & Aquaculture 30, no. 2: 195–214.
Seesholtz, A. M., M. J. Manuel, and J. P. Van Eenennaam. 2015. “First
Documented Spaw ning and Associated Habitat Conditions for Green
Sturgeon in the Feather River, California.” Environmental Biology of
Fishes 98: 905–912.
Smith, A., K. E. Smokorowski, and M. Power. 2017. “Spawning Lake
Sturgeon (Acipenser fulvescens Rafinesque, 1817) and Their Habitat
Characteristics in Rainy River, Ontario and Minnesota.” Journal of
Applied Ichthyology 33, no. 3: 328–337.
Smith, J. A., H. J. Flowers, and J. E. Hightower. 2015. “Fall Spawning of
Atlantic Sturgeon in the Roanoke River, North Carolina.” Transactions
of the American Fisheries Society 144, no. 1: 48–54.
Spear, M. C., and J. D. Kieffer. 2016. “Critical Thermal Maxima and
Hematology for Juvenile Atlantic (Acipenser oxyrinchus Mitchill 1815)
and Shortnose (Acipenser brevirostrum Lesueur, 1818) Sturgeons.”
Journal of Applied Ichthyology 32, no. 2: 251–257.
Struthers, D. P., L. F. Gutowsky, E. C. Enders, et al. 2017. “Factors
Influencing the Spatial Ecology of Lake Sturgeon and Walleye Within
an Impounded Reach of the Winnipeg River.” Environmental Biolog y of
Fishes 100: 1085–1103.
Sulak, K. J., and J. P. Clugston. 1998. “Early Life History Stages of Gulf
Sturgeon in the Suwanne e River, Florida.” Transac tions of the Ameri can
Fisheries Society 127, no. 5: 758–771.
Taubert, B. D. 1980. “Reproduction of Shortnose Sturgeon (Acipenser
brevirostrum) in Holyoke Pool, Connecticut River, Massachusetts.”
Copeia: 114–117.
Taylor, A. D., K. Ohashi, J. Sheng, and M. K. Litvak. 2016. “Oceanic
Distribution, Behaviour, and a Winter Aggregation Area of Adult
Atlantic Sturgeon, Acipenser oxyrinchus oxyrinchus, in the Bay of
Fundy, Canada.” PLoS One 11, no. 4: e0152470.
Taylor, A. D., and M. K. Lit vak. 2017. “Timing and L ocation of Spawning
Based on Larval Capture and Ultrasonic Telemetry of Atlantic St urgeon
in the Saint John River, New Brunswick.” Transactions of the Amer ican
Fisheries Society 146, no. 2: 283 –290.
Thiem, J. D., D. Hatin, P. Dumont, G. Van Der Kraak, and S. J. Cooke.
2013. “Biology of Lake Sturgeon (Acipenser fulvescens) Spawning Below
a Dam on the Richelieu River, Quebec: Behaviour, Egg Deposition, and
Endocrinology.” Canadian Journal of Zoology 91, no. 3: 175–186.
Trested, D. G., K. Ware, R. Bakal, and J. J. Isely. 2011. “Microhabitat
Use and Seasonal Movements of Hatchery- Reared and Wild Shortnose
Sturgeon in the Savannah River, South Carolina– Georgia.” Journal of
Applied Ichthyology 27, no. 2: 454–461.
Usvyatsov, S., J. Picka, R. S. Hardy, T. D. Shepherd, J. Watmough, and
M. K. Litvak. 2012. “Modeling the Timing of Spawning and Hatching
of Shortnose Sturgeon, Acipenser brevirostrum, in the Saint John River,
New Brunswick, Canada.” Canadian Journal of Fisheries and Aquatic
Sciences 69, no. 8: 1316–1328.
Usvyatsov, S., J. Picka, A. Taylor, J. Watmough, and M. K. Litvak. 2013.
“Timing and Extent of Drift of Shortnose Sturgeon Lar vae in the Saint
John River, New Brunswick, Canada.” Transactions of the American
Fisheries Society 142, no. 3: 717–730.
Van Eenennaam, J. P., J. Linares- Casenave, X . Deng, and S. I. Doroshov.
2005. “Effect of Incubation Temperature on Green Sturgeon Embr yos,
Acipenser medirostris.” Environmental Biology of Fishes 72: 145–154.
Verhille, C. E., S . Lee, A. E. Todgh am, D. E. Cocherell, S. S . Hung, and N.
A. Fangue. 2016. “Effects of Nutritional Deprivation on Juvenile Green
Sturgeon Grow th and Thermal Tolerance.” Environmental Biology of
Fishes 99: 145–159.
Vine, J. R., S. C. Holbrook, W. C. Post, and B. K. Peoples. 2019.
“Identifying Environmental Cues for Atlantic Sturgeon and Shortnose
Sturgeon Spaw ning Migrations in the Savannah River.” Transactions of
the American Fisheries Society 148, no. 3: 671–681.
Wang, Y. L., F. P. Binkowski, and S. I. Doroshov. 1985. “Effect of
Temperature on Early Development of White and Lake Sturgeon,
Acipenser transmontanus and A. fulvescens.” Environmental Biolog y of
Fishes 14: 43 –50.
Wang, Y. L., R. K. Buodington, and S. I. Doroshov. 1987. “Influence
of Temperature on Yolk Utilization by the White Sturgeon, Acipenser
transmontanus.” Journal of Fish Biology 30, no. 3: 263–271.
Watson, L. R., A. Milani, and R. P. Hedrick. 1998. “Effects of Water
Temperature on Experimentally- Induced Infections of Juvenile
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
24 of 24 Global Change Biology, 2024
White Sturgeon (Acipenser transmontanus) With the White Sturgeon
Iridovirus (WSIV).” Aquaculture 166, no. 3–4: 213–228.
Webb, M. A., J. P. Van Eenennaam, S. I. Doroshov, and G. P. Moberg.
1999. “Preliminar y Observations on the Ef fects of Holding Temperature
on Reproductive Performance of Female White Sturgeon, Acipenser
transmontanus Richardson.” Aquaculture 176, no. 3- 4: 315–329.
Webb, M. A., J. P. Van Eenennaam, G. W. Feist, et al. 2001. “Effects
of Thermal Regime on Ovarian Maturation and Plasma Sex Steroids in
Farmed White Sturgeon, Acipenser transmontanus.” Aquaculture 201,
no. 1- 2: 137–151.
Weber, T. A., A. M. Dichiera, and C. J. Brauner. 2024. “Resetting
Thermal Limits: 10- Year- Old White Sturgeon Display Pronounced but
Reversible Thermal Plasticity.” Journal of Thermal Biology 119 : 10380 7.
Weber, W., C. A. Jennings, and S. G. Rogers. 1998. “Population Size
and Movement Patterns of Shortnose Sturgeon in the Ogeechee River
System, Georgia.” Proceedings of the Annual Conference of the Southeast
Association of Fish and Wildlife Agencies 52: 18 –28.
Werner, I., J. Linares- Casenave, J. P. Van Eenennaam, and S. I.
Doroshov. 2007. “The Effect of Temperature Stress on Development and
Heat- Shock Protein Expression in Larval Green Sturgeon (Acipenser
mirostris).” Environmental Biology of Fishes 79: 191–200.
Wilkes, P. A. 2011. “Thermal tolerance of lake sturgeon.” Doctoral
Dissertation, University of Georgia.
Wippelhauser, G. S., G. B. Zydlewski, M. Kieffer, J. Sulikowski, and
M. T. Kinnison. 2015. “Shortnose Sturgeon in the Gulf of Maine: Use
of Spawning Habitat in the Kennebec System and Response to Dam
Removal.” Transactions of the American Fisheries Society 144, no. 4:
742–752.
Wippelhauser, G. S., J. Sulikowski, G. B. Zydlewski, M. A. Altenritter,
M. Kieffer, and M. T. Kinnison. 2017. “Movements of Atlantic Sturgeon
of the Gulf of Maine Inside and Outside of the Geographically Defined
Distinct Population Segment.” Marine and Coastal Fisheries 9, no. 1:
93 –10 7.
Wood Environment & Infrastructure Solutions. 2016. Middle Columbia
River White Sturgeon Spawning Monitoring. B.C. Hydro.
Wooley, C. M., and E. J. Crateau. 1985. “Movement, Microhabitat,
Exploitation, a nd Management of Gulf of Mexico St urgeon, Apalach icola
River, Florida.” North American Journal of Fisheries Management 5, no.
4: 590–605.
Yoon, G. R., W. S. Bugg, F. Fehrmann, M. E. Yusishen, M. Suh, and W.
G. Anderson. 2022. “Long- term Effects of Temperature During Early
Life on Growth and Fatty Acid Metabolism in Ae- 0 Lake Sturgeon
(Acipenser fulvescens).” Journal of Thermal Biolog y 105: 103210.
Yoon, G. R., D. Deslauriers, E. C. Enders, J. R. Treberg, and W. G.
Anderson. 2019. “Effects of Temperature, Dissolved Oxygen, and
Substrate on the Development of Metabolic Phenotypes in Age- 0
Lake Sturgeon (Acipenser fulvescens): Implications for Overwintering
Survival.” Canadian Journal of Fisheries and Aquatic Sciences 76, no.
9: 1596–1607.
Yoon, G. R., L. Groening, C. N. Klassen, C. Brandt, and W. G. Anderson.
2022. “Long- Term Effects of Temperature on Grow th, Energ y Density,
Whole- Body Composition and Aerobic Scope of Age- 0 Lake Sturgeon
(A. fulvescens).” Aquaculture 547: 737505.
Yusishen, M. E., G. R. Yoon, W. Bugg, K. M. Jeffries, S. Currie, and W.
G. Anderson. 2020. “Love thy Neighbor: Social Buffering Following
Exposure to an Acute Thermal Stressor in a Gregarious Fish, the
Lake Sturgeon (Acipenser fulvescens).” Comparative Biochemistr y and
Physiolog y Part A: Molecular & Integrative Physiology 243: 110686.
Zhang, Y., and J. D. Kieffer. 2017. “The Effect of Temperature on the
Resting a nd Post- Exercise Met abolic Rates and Aerobic Metabolic Scope
in Shortnose Sturgeon Acipenser brevirostrum.” Fish Physiolog y and
Biochemistry 43: 1245–1252.
Zhang, Y., and J. D. Kieffer. 2014. “Critica l Thermal Maxi mum (CTmax)
and Hematology of Shortnose Sturgeons (Acipenser brevirostrum)
Acclimated to Three Temperatures.” Canadian Journal of Zoology 92,
no. 3: 215–221.
Zhang, Y., J. R. Loughery, C. J. Martyniuk, and J. D. Kieffer. 2017.
“Physiological a nd Molecular R esponses of Juvenile Shortnos e Sturgeon
(Acipenser brevirostrum) to Thermal Stress.” Comparative Biochemistry
and Physiology Part A: Molecular & Integrative Physiolog y 203: 314–321.
Ziegeweid, J. R., C. A. Jennings, and D. L. Peterson. 2008. “ Thermal
Maxima for Juvenile Shortnose Sturgeon Acclimated to Different
Temp eratures .” Environmental Biology of Fishes 82: 299–30 7.
Supporting Information
Additional supporting information can be found online in the
Supporting Information section.
13652486, 2024, 11, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17564, Wiley Online Library on [21/11/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ResearchGate has not been able to resolve any citations for this publication.
Article
Full-text available
Amphibians and fishes play a central role in shaping the structure and function of freshwater environments. These organisms have a limited capacity to disperse across different habitats and the thermal buffer offered by freshwater systems is small. Understanding determinants and patterns of their physiological sensitivity across life history is, therefore, imperative to predicting the impacts of climate change in freshwater systems. Based on a systematic literature review including 345 experiments with 998 estimates on 96 amphibian (Anura/Caudata) and 93 freshwater fish species (Teleostei), we conducted a quantitative synthesis to explore phylogenetic, ontogenetic, and biogeographic (thermal adaptation) patterns in upper thermal tolerance (CT max ) and thermal acclimation capacity (acclimation response ratio, ARR) as well as the influence of the methodology used to assess these thermal traits using a conditional inference tree analysis. We found globally consistent patterns in CT max and ARR, with phylogeny (taxa/order), experimental methodology, climatic origin, and life stage as significant determinants of thermal traits. The analysis demonstrated that CT max does not primarily depend on the climatic origin but on experimental acclimation temperature and duration, and life stage. Higher acclimation temperatures and longer acclimation times led to higher CT max values, whereby Anuran larvae revealed a higher CT max than older life stages. The ARR of freshwater fishes was more than twice that of amphibians. Differences in ARR between life stages were not significant. In addition to phylogenetic differences, we found that ARR also depended on acclimation duration, ramping rate, and adaptation to local temperature variability. However, the amount of data on early life stages is too small, methodologically inconsistent, and phylogenetically unbalanced to identify potential life cycle bottlenecks in thermal traits. We, therefore, propose methods to improve the robustness and comparability of CT max /ARR data across species and life stages, which is crucial for the conservation of freshwater biodiversity under climate change.
Article
Full-text available
Evolutionary stasis characterizes lineages that seldom speciate and show little phenotypic change over long stretches of geological time. Although lineages that appear to exhibit evolutionary stasis are often called living fossils, no single mechanism is thought to be responsible for their slow rates of morphological evolution and low species diversity. Some analyses of molecular evolutionary rates in a handful of living fossil lineages have indicated that they exhibit slow rates of genomic change. Here, we investigate mechanisms of evolutionary stasis using a dataset of 1,105 exons for 481 vertebrate species. We demonstrate that two ancient clades of ray-finned fishes classically called living fossils, gars and sturgeons, exhibit the lowest rates of molecular substitution in protein-coding genes among all jawed vertebrates. Comparably low rates of evolution are observed at fourfold degenerate sites in gars and sturgeons, implying a mechanism of stasis decoupled from selection that we speculate is linked to a highly effective DNA repair apparatus. We show that two gar species last sharing common ancestry over 100 million years ago produce morphologically intermediate and fertile hybrids in the wild. This makes gars the oldest naturally hybridizing divergence among eukaryotes and supports a theoretical prediction that slow rates of nucleotide substitution across the genome slow the accumulation of genetic incompatibilities, enabling hybridization across deeply divergent lineages and slowing the rate of speciation over geological timescales. Our results help establish molecular stasis as a barrier to speciation and phenotypic innovation and provide a mechanism to explain the low species diversity in living fossil lineages.
Article
Full-text available
Evolutionary stasis characterizes lineages that seldom speciate and show little phenotypic change over long stretches of geological time. Although lineages that appear to exhibit evolutionary stasis are often called living fossils, no single mechanism is thought responsible for their slow rates of morphological evolution and low species diversity. Some analyses of molecular evolutionary rates in a handful of living fossil lineages have indicated they exhibit slow rates of genomic change. Here, we investigate mechanisms of evolutionary stasis using a dataset of 1,105 exons for 481 vertebrate species. We demonstrate that two ancient clades of ray-finned fishes classically called living fossils, gars and sturgeons, exhibit the lowest rates of molecular substitution in protein coding genes among all jawed vertebrates. Comparably low rates of evolution are observed at four-fold degenerate sites in gars and sturgeons, implying a mechanism of stasis decoupled from selection that we speculate is linked to a highly effective DNA repair apparatus. We show that two gar species last sharing common ancestry over 100 million years ago naturally produce morphologically intermediate and fertile hybrids. This makes gars the oldest naturally hybridizing divergence among eukaryotes and supports a theoretical prediction that slow rates of nucleotide substitution across the genome slows the accumulation of genetic incompatibilities, enabling hybridization across deeply divergent lineages and perhaps slowing the rate of speciation. Our results help establish molecular stasis as a barrier to speciation and phenotypic innovation and provide a mechanism to explain the low species diversity in living fossil lineages.
Article
Full-text available
Heatwaves are increasing in frequency and severity, posing a significant threat to organisms globally. In aquatic environments heatwaves are often associated with low environmental oxygen, which is a deadly combination for fish. However, surprisingly little is known about the capacity of fishes to withstand these interacting stressors. This issue is particularly critical for species of extreme conservation concern such as sturgeon. We assessed the tolerance of juvenile white sturgeon from an endangered population to heatwave exposure and investigated how this exposure affects tolerance to additional acute stressors. We measured whole-animal thermal and hypoxic performance and underlying epigenetic and transcriptional mechanisms. Sturgeon exposed to a simulated heatwave had increased thermal tolerance and exhibited complete compensation for the effects of acute hypoxia. These changes were associated with an increase in mRNA levels involved in thermal and hypoxic stress (hsp90a, hsp90b, hsp70 and hif1a) following these stressors. Global DNA methylation was sensitive to heatwave exposure and rapidly responded to acute thermal and hypoxia stress over the course of an hour. These data demonstrate that juvenile white sturgeon exhibit substantial resilience to heatwaves, associated with improved cross-tolerance to additional acute stressors and involving rapid responses in both epigenetic and transcriptional mechanisms.
Article
Full-text available
Although meta‐analysis has become an essential tool in ecology and evolution, reporting of meta‐analytic results can still be much improved. To aid this, we have introduced the orchard plot, which presents not only overall estimates and their confidence intervals, but also shows corresponding heterogeneity (as prediction intervals) and individual effect sizes. Here, we have added significant enhancements by integrating many new functionalities into orchaRd 2.0. This updated version allows the visualisation of heteroscedasticity (different variances across levels of a categorical moderator), marginal estimates (e.g. marginalising out effects other than the one visualised), conditional estimates (i.e. estimates of different groups conditioned upon specific values of a continuous variable) and visualisations of all types of interactions between two categorical/continuous moderators. orchaRd 2.0 has additional functions which calculate key statistics from multilevel meta‐analytic models such as I² and R². Importantly, orchaRd 2.0 contributes to better reporting by complying with PRISMA‐EcoEvo (preferred reporting items for systematic reviews and meta‐analyses in ecology and evolution). Taken together, orchaRd 2.0 can improve the presentation of meta‐analytic results and facilitate the exploration of previously neglected patterns. In addition, as a part of a literature survey, we found that graphical packages are rarely cited (~3%). We plea that researchers credit developers and maintainers of graphical packages, for example, by citations in a figure legend, acknowledging the use of relevant packages.
Article
Full-text available
Climate change-induced warming effects are already evident in river ecosystems, and projected increases in temperature will continue to amplify stress on fish communities. In addition, many rivers globally are impacted by dams, which have many negative effects on fishes by altering flow, blocking fish passage, and changing sediment composition. However, in some systems, dams present an opportunity to manage river temperature through regulated releases of cooler water. For example, there is a government mandate for Kenney dam operators in the Nechako river, British Columbia, Canada, to maintain river temperature <20°C in July and August to protect migrating sockeye salmon (Oncorhynchus nerka). However, there is another endangered fish species inhabiting the same river, Nechako white sturgeon (Acipenser transmontanus), and it is unclear if these current temperature regulations, or timing of the regulations, are suitable for spawning and developing sturgeon. In this study, we aimed to identify upper thermal thresholds in white sturgeon embryos and larvae to investigate if exposure to current river temperatures are playing a role in recruitment failure. We incubated embryos and yolk-sac larvae in three environmentally relevant temperatures (14, 18 and 21°C) throughout development to identify thermal thresholds across different levels of biological organization. Our results demonstrate upper thermal thresholds at 21°C across physiological measurements in embryo and yolk-sac larvae white sturgeon. Before hatch, both embryo survival and metabolic rate were reduced at 21°C. After hatch, sublethal consequences continued at 21°C because larval sturgeon had decreased thermal plasticity and a dampened transcriptional response during development. In recent years, the Nechako river has reached 21°C by the end of June, and at this temperature, a decrease in sturgeon performance is evident in most of the traits measured. As such, the thermal thresholds identified here suggest current temperature regulations may not be suitable for developing white sturgeon and future recruitment.
Article
Full-text available
Acoustic telemetry allows for fine-scale, or positional, tracking of fish in localised environments, and advancement in analytical techniques allows for quantifiable patterns in fish movement and behaviour. White sturgeon Acipenser transmontanus in the regulated Upper Columbia River are listed as endangered in Canada due to their considerable decline over the last century. An improved understanding of where, when, and why white sturgeon move in relation to river regulation is important for species recovery. A VEMCO Positioning System was used to collect the positions of white sturgeon in critical habitats immediately downstream of a dam on the Upper Columbia River over a 1 yr period. We applied hidden Markov models and generalised linear mixed models to (1) identify ecologically meaningful movement behaviours within the positions dataset; and (2) investigate the relationships between movement behaviour and biological (sex) and environmental (e.g. discharge, temperature, habitat) factors. Two behaviour states were identified: ‘residential’, characterised by short movements with less frequent turns, and ‘exploratory’, characterised by longer movements with more frequent turns. Water temperature largely influenced the mean weekly probability of a behaviour state, while discharge influenced the spatial distribution of movement behaviours. Changes in movement patterns were also apparent across seasons, with a higher occurrence of residential behaviour in the winter and spring and exploratory behaviour in the summer and fall. Results will help inform species recovery measures, such as overall flow management and optimization of operations to reduce impacts of river regulation.
Article
Freshwater fish such as white sturgeon (Acipenser transmontanus) are particularly vulnerable to the effects of anthropogenically induced global warming. Critical thermal maximum tests (CTmax) are often conducted to provide insight into the impacts of changing temperatures; however, little is known about how the rate of temperature increase in these assays affects thermal tolerance. To assess the effect of heating rate (0.3 °C/min, 0.03 °C/min, 0.003 °C/min) we measured thermal tolerance, somatic indices, and gill Hsp mRNA expression. Contrary to what has been observed in most other fish species, white sturgeon thermal tolerance was highest at the slowest heating rate of 0.003 °C/min (34.2 °C, and CTmax of 31.3 and 29.2 °C, for rates 0.03 and 0.3 °C/min, respectively) suggesting an ability to rapidly acclimate to slowly increasing temperatures. Hepatosomatic index decreased in all heating rates relative to control fish, indicative of the metabolic costs of thermal stress. At the transcriptional level, slower heating rates resulted in higher gill mRNA expression of Hsp90a, Hsp90b, and Hsp70. Hsp70 mRNA expression was increased in all heating rates relative to controls, whereas expression of Hsp90a and Hsp90b mRNA only increased in the two slower trials. Together these data indicate that white sturgeon have a very plastic thermal response, which is likely energetically costly to induce. Acute temperature changes may be more detrimental to sturgeon as they struggle to acclimate to rapid changes in their environment, however under slower warming rates they demonstrate strong thermal plasticity to warming.
Article
Chronic exposure to high temperatures may leave freshwater fishes vulnerable to opportunistic pathogens, particularly during early life stages. Lake sturgeon, Acipenser fulvescens, populations within the northern expanse of their range in Manitoba, Canada, may be susceptible to high temperature stress and pathogenic infection. We acclimated developing lake sturgeon for 21 days to two ecologically-relevant, summer temperatures (16 and 20°C). Individuals from both acclimation treatments were then exposed to 0, 30, and 60 µg.ml-1 bacterial lipopolysaccharides (endotoxins), as an immune stimulus, for 48 h and sampled 4 and 48 h during trial exposures and following a 7-day recovery period. We then measured whole body transcriptional (mRNA) responses involved in the innate immune, stress, and fatty acid responses following acute exposure to the bacterial endotoxins. Data revealed that overall levels of mRNA transcript abundance were higher in 20°C reared sturgeon under control conditions. However, following exposure to a bacterial stimulus, lake sturgeon acclimated to 16°C produced a more robust and persistent transcriptional response with higher mRNA transcript abundance across innate immune, stress, and fatty acid responses than their 20°C acclimated counterparts. Additional whole-animal performance metrics (critical thermal maximum, metabolic rate, cortisol concentration, and whole-body and mucosal lysozyme activity) demonstrated acclimation-specific responses, indicating compromised metabolic, stress, and enzymatic capacity following the initiation of immune related responses. Our study showed that acclimation to 20°C during early development impaired the immune capacity of developing lake sturgeon as well as the activation of molecular pathways involved in the immune, stress, and fatty acid responses. The present study highlights the effects of ecologically-relevant, chronic thermal stress on seasonal pathogen susceptibility in this endangered species.