Download the response of echinoderms to ocean acidification

THE RESPONSE OF ECHINODERMS
TO OCEAN ACIDIFICATION
CO2SCIENCE & SPPI ORIGINAL PAPER ♦
September 9, 2015
THE RESPONSE OF ECHINODERMS TO OCEAN WARMING
Citation: Center for the Study of Carbon Dioxide and Global Change. “The Response of Echinoderms to Ocean
Acidification.” Last modified Sep. 9, 2015. http://www.co2science.org/subject/o/summaries/acidechinoderms.php.
As the air’s CO2 content rises in response to ever-increasing anthropogenic CO2 emissions, and
as more and more carbon dioxide therefore dissolves in the surface waters of the world’s oceans,
theoretical reasoning suggests the pH values of the planet’s oceanic waters should be gradually
dropping. The IPCC and others postulate that this chain of events, commonly referred to as ocean
acidification, will cause great harm -- and possibly death -- to marine life in the decades and
centuries to come. However, as ever more pertinent evidence accumulates, a much more
optimistic viewpoint is emerging. This summary examines the topic of the potential impacts of
ocean acidification on echinoderms.
According to Dupont et al. (2010)1, “echinoderms are among the most abundant and ecologically
successful groups of marine animals (Micael et al., 2009), and are one of the key marine groups
most likely to be impacted by predicted climate change events,” presumably because “the larvae
and/or adults of many species from this phylum form skeletal rods, plates, test, teeth, and spines
from an amorphous calcite crystal precursor, magnesium calcite, which is 30 times more soluble
than normal calcite (Politi et al., 2004),” and this fact would normally be thought to make it much
more difficult for them (relative to most other calcifying organisms) to produce calcificationdependent body parts.
Working with naturally-fertilized eggs of the
common sea star Crossaster papposus, which they
collected and transferred to five-liter culture
aquariums filled with filtered seawater (a third of
which was replaced every four days), Dupont et al.
thus tested this hypothesis by regulating the pH of
the tanks to values of either 8.1 or 7.7 by adjusting
environmental CO2 levels to either 372 ppm or 930
ppm, during which time they documented
settlement success as the percentage of initially
free-swimming larvae that affixed themselves to
the aquarium walls, larval length at various time
intervals, and degree of calcification. In doing so
the three researchers report that just the opposite
of what is often predicted actually happened, as
the echinoderm larvae and juveniles were
“positively impacted by ocean acidification.” More
specifically, they found that “larvae and juveniles
raised at low pH grow and develop faster, with no
negative effect on survival or skeletogenesis
1
In fact, they state that the
sea stars’ growth rates were
“two times higher” in the
acidified seawater; and they
remark that “C. papposus
seem to be not only more
than simply resistant to
ocean acidification, but are
also performing better.”
http://www.co2science.org/articles/V13/N34/B3.php
2
within the time frame of the experiment (38 days).” In fact, they state that the sea stars’ growth
rates were “two times higher” in the acidified seawater; and they remark that “C. papposus seem
to be not only more than simply resistant to ocean acidification, but are also performing better.”
The Swedish scientists conclude that “in the future ocean, the direct impact of ocean acidification
on growth and development potentially will produce an increase in C. papposus reproductive
success,” and that “a decrease in developmental time will be associated with a shorter pelagic
period with a higher proportion of eggs reaching settlement,” leading the sea stars to become
“better competitors in an unpredictable environment.” Such favorable findings are surprising,
especially for a creature that makes its skeletal rods, plates, test, teeth, and spines from a
substance that is 30 times more soluble than normal calcite.
Schram et al. (2011)2 investigated the impacts of ocean acidification on another sea star, Luidia
clathrata. In their experiment, “two groups of sea stars, each with two arms excised, were
maintained on a formulated diet in seawater bubbled with air alone (pH 8.2, approximating a
pCO2 of 380 ppm) or with a controlled mixture of air/CO2 (pH 7.8, approximating a pCO2 of 780
ppm),” while “arm length, total body wet weight, and righting responses were measured
weekly.” Then, after 97 days, which they describe as “a period of time sufficient for 80% arm
regeneration,” they say that “protein, carbohydrate, lipid and ash levels were determined for
body wall and pyloric caecal tissues of intact and regenerating arms of individuals held in both
seawater pH treatments.”
In describing their findings, the four U.S. researchers report that “adults of the common soft
bottom predatory sea star Luidia clathrata exposed to end-of-century conditions of ocean
acidification (pH 7.8) are relatively unimpaired in their regenerative capacity,” which
“encompasses not only their ability to re-grow their arms, but their ability to allocate materials
and energy to regenerated somatic body components.” In addition, they say “there is no
discernable pattern arising from exposure to a reduced seawater pH of 7.8 for 97 days on righting
behavior,” which they say is “an integrative measure of stress.” Schram et al. conclude the report
of their work by stating that “the demonstration of an organism’s ability to sustain normal
functions under these conditions is as equally important to document as those that are negatively
impacted,” since “this information will be critical to future assessments of prospective impacts
of ocean acidification at the community level.”
In prefacing their work, Schlegel et al. (2012)3 write that “environmental factors directly affect
populations by selecting resilient individuals,” noting that “selection at the gametic level, or
during early life, has strong and immediate effects at the population level, carrying over into
subsequent life stages,” such that “heritability of this resilience leads to cascading adaptive
effects in subsequent generations.” And as an example of this process, they report that “in freespawning marine organisms, sperm selection during fertilization plays a key role by determining
the nature and diversity of genotypes in the subsequent generation (Levitan, 1996; 2008) and
thus their resilience to environmental change.”
2
3
http://www.co2science.org/articles/V15/N4/B2.php
http://www.co2science.org/articles/V16/N30/C3.php
3
Against this backdrop, Schlegel et al. investigated “the effects of CO2-induced ocean acidification
on the early life history stages in the Australasian sea urchin Heliocidaris erythrogramma,
focusing on intra-specific variation in responses, which can be highly variable for this species
(Evans and Marshall, 2005).” More specifically, and “following the A1FI-scenario from the IPCC’s
4th assessment report,” they “compared the effects of present day conditions for southeast
Australia with the end-of-century scenario (pCO2=970 ppm; pH=0.3 unit reduction) and a highCO2 scenario (pCO2=1600 ppm; pH=0.5 unit reduction),” after which the “observed effects on
sperm swimming behavior were applied within an established fertilization kinetics modeling
framework (Vogel et al., 1982; Styan et al., 2008) to predict fertilization outcomes of single urchin
pairs at each pCO2 level.” Last of all, these results “were then compared to observed results from
fertilization experiments conducted in the laboratory.”
It is likely that “ocean
acidification will lead to
selection against susceptible
phenotypes as well as to rapid
fixation of alleles that allow
reproduction under more
acidic conditions,” which
phenomena “may ameliorate
the biotic effects of climate
change if taxa have sufficient
extant genetic variation upon
Results of the analysis indicated that “acidification
significantly decreased the proportion of motile
sperm but had no effect on sperm swimming speed,”
and the four researchers went on to state that the
subsequent fertilization experiments “showed
strong inter-individual variation in responses to
ocean acidification, ranging from a 44% decrease to
a 14% increase in fertilization success.”
In commenting on their findings, Schlegel et al.
opined that their results suggest that “some
individuals will exhibit enhanced fertilization success
in acidified oceans, supporting the concept of
‘winners’ and ‘losers’ of climate change at an
individual level.” And they say that if these
differences are heritable, it is likely that “ocean
acidification will lead to selection against susceptible
phenotypes as well as to rapid fixation of alleles that
allow reproduction under more acidic conditions,”
which phenomena “may ameliorate the biotic
effects of climate change if taxa have sufficient
extant genetic variation upon which selection can
act.”
which selection can act.”
Real world data supporting phenotypic adaptation
to seawater of lower pH was provided by Moulin et
al. (2011)4, who conducted a field experiment on the
sea urchin Paracentrotus lividus in an attempt “to compare the effect of pH on the progeny of
individuals collected from the same shore, i.e., same population, but from distinct tide pools: one
where night pH was significantly reduced and the other where this decline was not so important.”
In doing so, the four Belgian researchers report that the pH of coastal seawater at the site they
studied (Aber, Crozon peninsula, southern Brittany, France) was 8.14; but they say that at the
4
http://www.co2science.org/articles/V14/N42/B1.php
4
end of the night low tides, tide pools 1 (subtidal) and 2 (intertidal) had pH values of, respectively,
7.8 and 7.4. Under these conditions, they detected “no significant difference in gonad maturity
between individuals from the two tide pools,” and they report that “the offspring of sea urchins
from the tide pool with higher pH decrease (tide pool 2) showed a better resistance to
acidification at pH 7.4 than that of sea urchins from the tide pool with low pH decrease (tide pool
1) in terms of fertilization, viz. a reduction of over 30% [for tide pool 1] compared to about 20%
for tide pool 2.” Commenting on their findings, Moulin et al. conclude that “sea urchins inhabiting
stressful intertidal environments produce offspring that may better resist future ocean
acidification.” And they add that the fact that “the fertilization rate of gametes whose progenitors
came from the tide pool with higher pH decrease was significantly higher,” suggests “a possible
acclimation or adaptation of gametes to pH stress.”
Also studying Paracentrotus lividus was Martin et al. (2011)5, who write that “ocean acidification
is predicted to have significant effects on benthic calcifying invertebrates, in particular on their
early developmental states,” and they note that “echinoderm larvae could be particularly
vulnerable to decreased pH, with major consequences for adult populations.” Against this
backdrop the authors explored the effect of a gradient of decreasing pH from 8.1 to 7.0 -corresponding to atmospheric CO2 concentrations of ~400 ppm to ~6630 ppm -- on the larvae of
the sea urchin Paracentrotus lividus, a common but economically and ecologically important
species that is widely distributed throughout the Mediterranean Sea and the northeast Atlantic
from Ireland to southern Morocco. This was accomplished using “multiple methods to identify
the response of P. lividus to CO2-driven ocean acidification at both physiological (fertilization,
growth, survival and calcification) and molecular (expression of genes involved in calcification
and development) levels.”
Results indicated that “Paracentrotus lividus appears to be extremely resistant to low pH, with
no effect on fertilization success or larval survival.” They did, however, discover that “larval
growth was slowed when exposed to low pH,” such that larvae of P. lividus “collected at pH 7.5
at 46 hours post-fertilization (real age) were smaller than in the control treatment [pH 8.1] and
corresponded to a virtual age of 36 hours (a delay in development of 10 hours).” Continuing, they
further indicate that “down to a pH of 7.25, the larvae at Day 3 have a normal morphology but
are delayed in development,” such that the apparent decrease in calcification at that point in
time is, as they put it, “simply an indirect consequence of the impact of low pH on developmental
rate.” Or in other words, as they continue, “at a given developmental state (or size), larvae
present the same calcium incorporation rate regardless of pH.” They also report that “genes
involved in development and biomineralization were upregulated by factors of up to 26 at low
pH,” which suggests “plasticity at the gene expression level” in P. lividus that “allows a normal,
but delayed, development under low pH conditions.”
Introducing their study, Ericson et al. (2010)6 write that in polar latitudes “the effects of changing
pCO2 and pH on gametes may be influenced by the carbonate chemistry of cold water, such as
the already higher pCO2 and lower seawater pH,” and they say “it has also been predicted that
ocean acidification effects on organisms may be more apparent and appear earliest in polar
5
6
http://www.co2science.org/articles/V14/N18/B3.php
http://www.co2science.org/articles/V14/N21/B1.php
5
waters.” To explore this situation further, Ericson et al. “investigated the effects of present-day
pH 8.0, predicted ocean surface pH for the years 2100 and 2300 (pH 7.7 and pH 7.3, respectively)
and an extreme pH (pH 7.0) on fertilization and embryogenesis in the Antarctic nemertean worm
Parborlasia corrugatus and sea urchin Sterechinus neumayeri.”
According to the four researchers, results indicated that “fertilization success was not affected
by pH in P. corrugatus across a range of sperm concentrations,” and that “fertilization success in
S. neumayeri declined significantly in pH 7.0 and 7.3 seawater, but only at low sperm
concentration.” In addition, they say that “seawater pH had no effect on the rate of egg cleavage
in S. neumayeri, or the proportion of abnormal embryos 1-day post-fertilization,” and that “P.
corrugatus embryogenesis was also relatively robust to pH changes, with a significant effect
detected only when the seawater pH was decreased to 7.0.” Given such findings, Ericson et al.
conclude, “as in a number of other studies (see reviews by Byrne et al., 2010; Dupont et al., 2010),
that gametes appeared relatively robust to pH change, especially to changes within the range
predicted for the near future (i.e. a decrease of 0.3-0.5 pH units),” and they state that their initial
findings “do not support a view that polar species are more affected by lowered pH compared
with temperate and tropical counterparts (as has also been shown for the later developmental
stages of S. neumayeri (Clark et al., 2009)).”
Yu et al. (2013)7 also studied Sterechinus neumayeri, as they too were concerned about how the
early life stages of this sea urchin are impacted by the levels of atmospheric CO 2 enrichment
being predicted to occur within the current century. Specifically, Yu et al. tested the effects of
high CO2/low pH on early development and larval growth by exposing them to environmental
levels of CO2 in McMurdo Sound (control: 410 ppm) and mildly elevated CO2 levels, both near the
level of the aragonite saturation horizon (510 ppm), and to under-saturating conditions (730
ppm). Under such conditions, the researchers report that over the course of development from
egg to late four-arm pluteus, they found that “(1) early embryological development was normal
with the exception of the hatching process, which was slightly delayed, (2) the onset of
calcification as determined by the appearance of CaCO3 spicule nuclei was on schedule, (3) the
lengths of the spicule elements, and the elongation of the spicule nuclei into the larval skeleton,
were significantly shorter in the highest CO2 treatment four days after the initial appearance of
the spicule nuclei, and (4) finally, without evidence of true developmental delay, larvae were
smaller overall under high CO2 treatments; and arm length, the most plastic morphological aspect
of the echinopluteus, exhibited the greatest response to high CO2/low pH/low carbonate
conditions.” As a result of these finding Yu et al. concluded that “effects of elevated CO2
representative of near future climate scenarios are proportionally minor on these early
development stages.”
Working with the purple sea urchin (Strongylocentrotus purpuratus), Yu et al. (2011)8 raised
larvae in seawater maintained at pCO2 levels ranging from ambient to 1,000 and 1,450 ppm CO2
(pH 7.7 and 7.5, respectively), while measuring, after three and six days development, “total
larval length (from the spicule tip of the postoral arm to the spicule tip of the aboral point) along
the spicules, to assess effects of low pH upwelling water on morphology.” Results indicated that
7
8
http://www.co2science.org/articles/V16/N25/B2.php
http://www.co2science.org/articles/V14/N32/B1.php
6
“even at the highest pCO2 treatments, larval development was normal in terms of timing and
morphological appearance,” although at both day 3 and 6 larvae in the 1450-ppm CO2 treatment
were 7-13% smaller than control larvae. Yu et al. also state that “the observed developmental
progression and survival of cultures was within the norm typically observed for this species at
this temperature range.” In addition, they indicate that “a lack of developmental deformities at
early stages for pCO2 ~1000 ppm has been previously reported for this species (Todgham and
Hofmann, 2009), and another local species, Lytechinus pictus, with a similar overlapping portion
of its range in southern California (O’Donnell et al., 2010).” And they say “there are even reports
that survival is increased in this species and its congener S. droebachiensis under some low pH
conditions (Dupont and Thorndyke, 2008).” Thus, it would appear, as Yu et al. conclude, that “the
effects of small magnitude in these urchin larvae are indicative of a potential resilience to nearfuture levels of ocean acidification.”
Also focusing on Strongylocentrotus purpuratus, Stumpp et al. (2011a)9 evaluated the impacts of
elevated seawater pCO2 (1264 ppm vs. 375 ppm) on the early development of, and the larval
metabolic and feeding rates of, this model marine organism. This was done via a protocol where
growth and development were assessed daily, for a period of three weeks, in terms of total body
length, body rod length, postoral rod length and posterolateral rod length, as well as mortality
and feeding and metabolic rates. Results of the analysis indicated that daily mortality rate (DMR)
was significantly higher under control conditions (DMR = 2.7% per day) in comparison to that
under high seawater pCO2 (DMR = 2.2% per day).
It was also observed, in the elevated CO2
But if comparisons are made
treatment, that larval development was about 8%
slower, such that it took slightly longer for
on the basis of development
equivalent development stages to be reached in
the high CO2 treatment.
stage, as was also done in this
As a result of the slower development of the
larvae in the high CO2 treatment, at any given
time the individuals in this treatment were found
to be smaller and less well developed than those
in the control treatment; and if that was the only
comparison to have been made in this study, the
effects of elevated CO2 might have been thought
to have been negative. But if comparisons are
made on the basis of development stage, as was
also done in this study, it would have been found
-- and was! -- that there were no long-term
physical differences between the larvae living in
the high and low CO2 treatments.
study, it would have been
found -- and was! -- that
there were no long-term
physical differences between
the larvae living in the high
and low CO2 treatments.
In light of these observations, it can be appreciated that in studies designed to reveal the effects
of atmospheric CO2 enrichment upon various species of marine life, treatment comparisons
should be made at equivalent development stages of the organism being studied; since at such
9
http://www.co2science.org/articles/V15/N15/B2.php
7
points along the life cycle of the purple sea urchin, there were no significant physical differences
between individuals raised in the control and CO2-enriched conditions. As Stumpp et al. thus
declare at the conclusion of their enlightening study, “we suggest that body length is a useful
scale of reference for studies in sea urchin larvae where a morphological delay in development
occurs,” and that “using time post-fertilization as a reference may lead to misinterpretation of
data,” i.e., to wrongfully assuming a negative result, when in reality there may be no deleterious
effect of ocean acidification. This is essentially the same conclusion reached by Stumpp et al.
(2011b) in a companion paper, where they say that “in studies in which a stressor induces an
alteration in the speed of development, it is crucial to employ experimental designs with a high
time resolution in order to correct for developmental artifacts,” which protocol “helps prevent
misinterpretation of stressor effects on organism physiology.”
Noting that “little is known about the adaptive capacity of species to respond to an acidified
ocean,” and, as a result, “predictions regarding future ecosystem responses remain incomplete,”
Pespeni et al. (2013)10 conducted a study that demonstrates that ocean acidification generates
striking patterns of genome-wide selection in purple sea urchins (Strongylocentrotus purpuratus)
cultured under different CO2 levels of 400 and 900
ppm. Working with seven different populations
The researchers conclude “our
collected along a 1,200-km mosaic of coastal
upwelling-driven acidification of the California
results demonstrate the
Current System, Pespeni et al. combined (1)
sequencing across the transcriptome of the purple
capacity for rapid evolution in
sea urchin, (2) growth measurements under
experimental acidification, and (3) tests of frequency
shifts in 19,493 polymorphisms during development,
the face of ocean acidification
while detecting in the process “the widespread
occurrence of genetic variation to tolerate ocean
and show that standing
acidification.”
genetic variation could be a
In describing their findings, the eleven researchers
report that although larval development and
reservoir of resilience to
morphology showed little response to elevated CO2,
they found “substantial allelic change in 40
climate change in this coastal
functional classes of proteins involving hundreds of
loci.” More particularly, they state that “pronounced
genetic changes, including excess amino acid
upwelling ecosystem.”
replacements, were detected in all populations and
occurred in genes for biomineralization, lipid
metabolism, and ion homeostasis - gene classes that build skeletons and interact in pH
regulation,” while noting that “such genetic change represents a neglected and important impact
of ocean acidification that may influence populations that show few outward signs of response
to acidification.” In considering all of the above, the researchers conclude “our results
demonstrate the capacity for rapid evolution in the face of ocean acidification and show that
10
http://www.co2science.org/articles/V16/N37/B3.php
8
standing genetic variation could be a reservoir of resilience to climate change in this coastal
upwelling ecosystem.”
Examining another species of urchin, Catarino et al. (2012)11 studied the development of larvae
produced by adults of the Arbacia dufresnei urchin, which they collected from a sub-Antarctic
population in the Straits of Magellan near Punta Arenas, Chile, when immersed in high (8.0),
medium (7.7) and low (7.4) pH seawater. The five scientists state their analysis showed that “the
proportion of abnormal larvae did not differ according to [pH] treatment,” with the result that
although “lower pH induced a delay in development” -- which has also been noted by Dupont et
al. (2010) -- it “did not increase abnormality.” They additionally indicate that “even at calcium
carbonate saturation states <<1, skeleton deposition occurred,” and they further note in this
regard that specimens of Heliocidaris erythrogramma also “seem not to be affected by a pH
decrease (until 7.6),” citing Byrne et al. (2009a,b), while likewise noting that the Antarctic
Sterechinus neumayeri is also thought to be “more robust to ocean acidification than tropical and
temperate sub-tidal species,” citing Clark et al. (2009) and Ericson et al. (2010). The findings of
Catarino et al., as well as those of the other researchers they cite, thus suggest that “polar and
sub-polar sea urchin larvae can show a certain degree of resilience to acidification.” And they
conclude that because of this fact, A. dufresnei has the potential to “migrate and further colonize
southern regions.”
Writing as background for their study, Sunday et al. (2011)12 state that the presumed acidification
of Earth’s oceans is predicted to impact marine biodiversity via “physiological effects impacting
growth, survival, reproduction and immunology, leading to changes in species abundances and
global distributions.” However, they note that “the degree to which these changes will play out
critically depends on the evolutionary rate at which populations will respond to natural selection
imposed by ocean acidification,” and they say that this phenomenon “remains largely
unquantified,” citing the work of Stockwell et al. (2003) and Gienapp et al. (2008). Against this
backdrop, working with a sea urchin species (Strongylocentrotus franciscanus) and a mussel
species (Mytilus trossulus) in a full-factorial breeding study, Sunday et al. measured the potential
for an evolutionary response to ocean acidification in the larval development rate of the two
coastal invertebrates.
In discussing their findings, the four researchers report their experiment revealed that “the sea
urchin species Stronglyocentrotus franciscanus has vastly greater levels of phenotypic and
genetic variation for larval size in future CO2 conditions compared to the mussel species Mytilus
trossulus,” and using these findings, they go on to demonstrate that “S. franciscanus may have
faster evolutionary responses within 50 years of the onset of predicted year-2100 CO2 conditions
despite having lower population turnover rates.” Sunday et al. conclude their study by saying
their comparisons suggest that “information on genetic variation, phenotypic variation, and key
demographic parameters, may lend valuable insight into relative evolutionary potentials across
a large number of species,” thereby also indicating that simplistic climate envelope models of
species redistributions in a future CO2-enriched and possibly warmer world are just not up to the
task of providing a picture of future biological reality. And they solidify this view by noting that
11
12
http://www.co2science.org/articles/V15/N23/B3.php
http://www.co2science.org/articles/V14/N46/B3.php
9
“a genetic basis for variation in CO2 responses
has been found in the three previous studies in
which it has been sought (Langer et al., 2009;
Parker et al., 2011; Pistevos et al., 2011),
supporting the notion that genetic variation
exists at some level for almost all quantitative
characters (Roff, 1997).”
Simplistic climate envelope
models of species redistributions
in a future CO2-enriched and
possibly warmer world are just
Introducing their work that was performed on
yet another urchin species, Moulin et al.
not up to the task of providing
(2014)13 note it has been suggested that in
numerous
marine
organisms
several
a picture of future biological
physiological processes may be directly or
indirectly impacted by the induced acidosis
reality.
and hypercapnia produced by continued
atmospheric CO2 enrichment; and they
indicate that species with low metabolism and inefficient ion regulatory abilities have been
suggested to be “more sensitive to a high seawater pCO2,” citing Melzner et al. (2009). In light of
these facts, Moulin et al. set forth to evaluate “the acid-base regulation of the coral reef sea
urchin Echinometra mathaei and the impact of decreased pH on its growth and respiration
activity,” which they did “in two identical artificial reef mesocosms during seven weeks,” when
the experimental tanks were maintained at mean pH values of 8.05 (standard) and 7.7
(“acidified”), together with “field-like night and day variations.”
Key among their findings, the five Belgian researchers report that “E. mathaei can regulate the
pH of its coelomic fluid in the considered range of pH.” As a result, Moulin et al. conclude that
this ability allows “a sustainable growth” and ensures “an unaffected respiratory metabolism, at
least at short term,” diminishing metabolism-based concerns for this marine species under
elevated CO2 conditions.
In an experiment designed to gain a better understanding of the effects of long-term exposure
of adult Echinometra sp. EE sea urchins native to the Red Sea’s Gulf of Aqaba, Hazan et al. (2014)14
studied specimens they collected there within eleven 37.5-liter glass aquariums they maintained
in equilibrium with air containing either 435 or 1,433 µatm of CO2 -- corresponding respectively
to seawater pH values of 8.1 and 7.7 -- for a period of eleven months, while they periodically
examined them for somatic and gonadal growth and skeletal microstructure, during which time
all urchins in the experiment completed full reproductive cycles typical of natural populations.
This work revealed that in the cases of (1) somatic and (2) gonadal growth, there were no
significant differences between the sea urchins maintained in the two CO2 treatments. They also
state that there was “no detectable impact of increased pCO2 on the [3] timing, [4] duration or
[5] progression of the cycle.” And they add that “scanning electron microscopy imaging of urchin
tests and spines revealed no signs of the usual observed effects of acidosis, such as [6] skeletal
13
14
http://www.co2science.org/articles/V17/oct/a29.php
http://www.co2science.org/articles/V18/feb/a19.php
10
dissolution, [7] widened stereo pores or [8] non-smoothed structures.” Taken together, these
several findings, in the words of the four researchers, “suggest high resistance of adult
Echinometra sp. EE to near future ocean acidification conditions.”
Finally, concluding with another longer-term study of ocean acidification (OA) effects on sea
urchins, Moulin et al. (2015)15 write that “due to their low metabolism and poor osmoregulation
abilities, sea urchins have been considered as victims of OA,” but they note that past studies of
the subject suggest that some adult sea urchins are able to maintain the pH of their coelomic
fluid when faced with a decrease of seawater pH, citing the work of Dupont and Thorndyke
(2012), Stumpp et al. (2012), Calosi et al. (2013), Collard et al. (2013, 2014), Moulin et al. (2014)
and Uthicke et al. (2014). However, they write that “previous studies exposed sea urchins brutally
to increased pCO2 levels whereas gradual acclimatization will better mimic future OA.” And they
also note that in all prior studies of post-metamorphic sea urchins: (1) the algae the urchins were
fed were supplied to them ad libitum, and (2) the algae had not been grown under OA conditions.
In their study, therefore, the Belgian researchers placed specimens of the sea urchin Echinometra
mathaei in “replicated mesocosms provided with an artificial reef consisting of hermatypic
scleractinians and reef calcareous substrate with its diverse communities of algae as principal
food,” after which the mesocosms experienced six months of gradual pH decrease until an OA
pH level of 7.7 was reached. These conditions were then maintained for seven additional months,
during which time a number of pertinent parameters were monitored, while at the conclusion of
the experiment the bio-mechanical resistance of the sea urchins’ skeletons was assessed.
After evaluating the many measurements they made of E. mathaei and its activities over the
course of their study, Moulin et al. (2015) concluded that the urchin appeared to be resilient to
ocean acidification levels expected to occur by 2100 in terms of “acid-base regulation, growth,
respiration rate and test mechanical properties,” all of which findings play a significant role in
determining the sea urchin’s interactions with both algae and corals.
In summation, with the passage of time, more and more evidence is accumulating that suggests
the impacts of ocean acidification on echinoderms may not be as bad as many initially thought.
Indeed, for many echinoderm species, the impacts will likely be minimal, if not altogether
positive.
REFERENCES
Anderson, A.J., Mackenzie, F.T. and Bates, N.R. 2008. Life on the margin: implications of ocean
acidification on Mg-calcite, high latitude and cold-water marine calcifiers. Marine Ecology
Progress Series 373: 265-273.
Bryne, M., Ho, M., Selvakumaraswamy, P., Nguyen, H.D., Dworjanyn, S.A. and Davis, A.R. 2009a.
Temperature, but not pH, compromises sea urchin fertilization and early development under
near-future climate change scenarios. Proceedings of the Royal Society B 276: 1883-1888.
15
http://www.co2science.org/articles/V18/may/a23.php
11
Byrne, M., Soars, N., Ho, M.A., Wong, E., McElroy, D., Selvakumaraswamy, P., Dworjanyn, S.A.
and Davis, A.R. 2010. Fertilization in a suite of coastal marine invertebrates from SE Australia is
robust to near-future ocean warming and acidification. Marine Biology 157: 2061-2069.
Bryne, M., Soars, N., Selvakumaraswamy, P., Dworjanyn, S.A. and Davis, A.R. 2009b. Sea urchin
fertilization in a warm, acidified and high pCO2 ocean across a range of sperm densities. Marine
Environmental Research 69: 234-239.
Calosi, P., Rastrick, S.P.S., Graziano, M., Thomas, S.C., Baggini, C., Carter, H., and Spicer, J.I. 2013.
Distribution of sea urchins living near shallow water CO2 vents is dependent upon species acidbase and ion-regulatory abilities. Marine Pollution Bulletin 73: 470-484.
Catarino, A.I., De Ridder, C., Gonzalez, M., Gallardo, P. and Dubois, P. 2012. Sea urchin Arbacia
dufresnei (Blainville 1825) larvae response to ocean acidification. Polar Biology 35: 455-461.
Clark, D., Lamare, M and Barker, M. 2009. Response of sea urchin pluteus larvae (Echinodermata:
Echinoidea) to reduced seawater pH: a comparison among a tropical, temperate, and a polar
species. Marine Biology 156: 1125-1137.
Collard, M., Laitat, K., Moulin, L., Catarino, A.I., Grosjean, Ph and Dubois, Ph. 2013. Buffer capacity
of the coelomic fluid in echinoderms. Comparative Biochemistry and Physiology Part A: Molecular
& Integrative Physiology 166: 199-206.
Collard, M., Dery, A., Dehairs, F. and Dubois, Ph. 2014. Euechinoidea and Cidaroidea respond
differently to ocean acidification. Comparative Biochemistry and Physiology Part A: Molecular &
Integrative Physiology 174: 45-55.
Dupont, S., Lundve, B. and Thorndyke, M. 2010. Near future ocean acidification increases growth
rate of the lecithotrophic larvae and juveniles of the sea star Crossaster papposus. Journal of
Experimental Zoology (Molecular and Developmental Evolution) 314B: 382-389.
Dupont, S., Ortega-Martinez, O. and Thorndyke, M. 2010. Impact of near-future ocean
acidification on echinoderms. Ecotoxicology 19: 449-462.
Dupont, S. and Thorndyke, M.C. 2008. Ocean acidification and its impacts on the early life-history
stages of marine animals. In: CIESM (Ed.). Impacts of Acidification on Biological, Chemical and
Physical Systems in the Mediterranean and Black Seas. Number 36 in CIESM Workshop
Monographs (F. Briand, Ed.), Monaco.
Dupont, S. and Thorndyke, M. 2012. Relationship between CO2-driven changes in extracellular
acid-base balance and cellular immune response in two polar echinoderm species. Journal of
Experimental Marine Biology and Ecology 424-425: 32-37.
Ericson, J.A., Lamare, M.D., Morley, S.A. and Barker, M.F. 2010. The response of two ecologically
important Antarctic invertebrates (Sterechinus neumayeri and Parborlasia corrugatus) to
12
reduced seawater pH: effects on fertilization and embryonic development. Marine Biology 157:
2689-2702.
Evans, J.P. and Marshall, D.J. 2005. Male-by-female interactions influence fertilization success
and mediate the benefits of polyandry in the sea urchin Heliocidaris erythrogramma. Evolution
59: 106-112.
Gayathri, S., Lakshminarayanan, R., Weaver, J.C., Morse, D.E., Kini, R.M. and Valiyaveettil, S. 2007.
In vitro study of magnesium-calcite biomineralization in the skeletal materials of the seastar
Pisaster giganteus. Chemistry - A European Journal 13: 3262-3268.
Gienapp, P., Teplitsky, C., Alho, J.S., Mills, J.A. and Merila, J. 2008. Climate change and evolution:
disentangling environmental and genetic responses. Molecular Ecology 17: 167-178.
Hazan, Y., Wangensteen, O.S. and Fine, M. 2014. Tough as a rock-boring urchin: adult
Echinometra sp. EE from the Red Sea show high resistance to ocean acidification over long-term
exposures. Marine Biology 161: 2532-2545.
Langer, G., Nehrke, G., Probert, I., Ly, J. and Ziveri, P. 2009. Strain-specific responses of Emiliania
huxleyi to changing seawater carbonate chemistry. Biogeosciences 6: 2637-2646.
Levitan, D.R. 1996. Effects of gamete traits on fertilization in the sea and the evolution of sexual
dimorphism. Nature 382: 153-155.
Levitan, D.R. 2008. Gamete traits influence the variance in reproductive success, the intensity of
sexual selection, and the outcome of sexual conflict among congeneric sea urchins. Evolution 62:
1305-1316.
Martin, S., Richier, S., Pedrotti, M.-L., Dupont, S., Castejon, C., Gerakis, Y., Kerros, M.-E.,
Oberhansli, F., Teyssie, J.-L., Jeffree, R. and Gattuso, J.-P. 2011. Early development and molecular
plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven
acidification. The Journal of Experimental Biology 214: 1357-1368.
Melzner, F., Gutowska, M.A., Langenbuch, M., Dupont, S., Lucassen, M., Thorndyke, M.C., Bleich,
M. and Portner, H.-O. 2009. Physiological basis for high CO2 tolerance in marine ectothermic
animals: pre-adaptation through lifestyle and ontogeny? Biogeosciences 6: 2313-2331.
Micael, J., Alves, M.J., Costa, A.C. and Jones, M.B. 2009. Exploitation and conservation of
echinoderms. Oceanography and Marine Biology 47: 191-208.
Moulin, L., Catarino, A.I., Claessens, T. and Dubois, P. 2011. Effects of seawater acidification on
early development of the intertidal sea urchin Paracentrotus lividus (Lamarck 1816). Marine
Pollution Bulletin 62: 48-54.
13
Moulin, L., Grosjean, P., Leblud, J., Batigny, A., Collard, M. and Dubois, P. 2015. Long-term
mesocosms study of the effects of ocean acidification on growth and physiology of the sea urchin
Echinometra mathaei. Marine Environmental Research 103: 103-114.
Moulin, L., Grosjean, P., Leblud, J., Batigny, A. and Dubois, P. 2014. Impact of elevated pCO 2 on
acid-base regulation of the sea urchin Echinometra mathaei and its relation to resistance to ocean
acidification: A study in Mesocosms. Journal of Experimental Marine Biology and Ecology 457:
97-104.
O’Donnell, M.J., Todgham, A.E., Sewell, M.A., Hammond, L.M., Ruggiero, K., Fangue, N.A., Zippay,
M.L. and Hofmann, G.E. 2010. Ocean acidification alters skeletogenesis and gene expression in
larval sea urchins. Marine Ecology Progress Series 398: 157-171.
Parker, L.M., Ross, P.M. and O’Connor, W.A. 2011. Populations of the Sydney rock oyster,
Saccostrea glomerata, vary in response to ocean acidification. Marine Biology 158: 689-697.
Pespeni, M.H., Sanford, E., Gaylord, B., Hill, T.M., Hosfelt, J.D., Jaris, H.K., LaVigne, M., Lenz, E.A.,
Russell, A.D., Young, M.K. and Palumbi, S.R. 2013. Evolutionary change during experimental
ocean acidification. Proceedings of the National Academy of Sciences USA 110: 6937-6942.
Pistevos, J.C.A., Calosi, P., Widdicombe, S. and Bishop, J.D.D. 2011. Will variation among genetic
individuals influence species responses to global climate change? Oikos 120: 675-689.
Politi, Y., Arod, T., Klein, E., Weiner, S. and Addadi, L. 2004. Sea urchin spine calcite forms via a
transient amorphous calcite carbonate phase. Science 306: 1161-1164.
Roff, D.A. 1997. Evolutionary Quantitative Genetics. Chapman and Hall, New York, New York,
USA.
Schlegel, P., Havenhand, J.N, Gillings, M.R. and Williamson, J.E. 2012. Individual variability in
reproductive success determines winners and losers under ocean acidification: A case study with
sea urchins. PLOS ONE 7: e53118.
Schram, J.B., McClintock, J.B., Angus, R.A and Lawrence, J.M. 2011. Regenerative capacity and
biochemical composition of the sea star Luidia clathrata (Say) (Echinodermata: Asteroidea) under
conditions of near-future ocean acidification. Journal of Experimental Marine Biology and Ecology
407: 266-274.
Stockwell, C.A., Hendry, A.P. and Kinnison, M.T. 2003. Contemporary evolution meets
conservation biology. Trends in Ecology and Evolution 18: 94-101.
Stumpp, M., Dupont, S., Thorndyke, M.C. and Melzner, F. 2011b. CO2 induced seawater
acidification impacts sea urchin larval development II: Gene expression patterns in pluteus larvae.
Comparative Biochemistry and Physiology, Part A 160: 320-330.
14
Stumpp, M., Trubenbach, K., Bennecke, D., Hu, M.Y. and Melzner, F. 2012. Resource allocation
and extracellular acid-base status in the sea urchin in response to CO2 induced seawater
acidification. Aquatic Toxicology 110-111: 194-207.
Stumpp, M., Wren, J., Melzner, F., Thorndyke, M.C. and Dupont, S.T. 2011a. CO2 induced
seawater acidification impacts sea urchin larval development I: Elevated metabolic rates
decrease scope for growth and induce developmental delay. Comparative Biochemistry and
Physiology, Part A 160: 331-340.
Styan, C.A., Kupriyanova, E. and Havenhand, J.N. 2008. Barriers to cross-fertilization between
populations of a widely dispersed polychaete species are unlikely to have arisen through gametic
compatibility arms-races. Evolution 62: 3041-3055.
Sunday, J.M., Crim, R.N., Harley, C.D.G. and Hart, M.W. 2011. Quantifying rates of evolutionary
adaptation in response to ocean acidification. PLoS ONE 6: e22881.
Todgham, A.E. and Hofmann, G.E. 2009. Transcriptomic response of sea urchin larvae,
Strongylocentrotus purpuratus, to CO2-driven seawater acidification. Journal of Experimental
Biology 212: 2579-2594.
Uthicke, S., Liddy, M.,Nguyen, H.D. and Byrne, M. 2014. Interactive effects of near-future
temperature increase and ocean acidification on physiology and gonad development in adult
Pacific sea urchin, Echinometra sp. A. Coral Reefs 33: 831-845.
Vogel, H., Czihak, G., Chang, P. and Wolf, W. 1982. Fertilization kinetics of sea urchin eggs.
Mathematical Biosciences 58: 189-216.
Yu, P.C., Matson, P.G., Martz, T.R. and Hofmann, G.E. 2011. The ocean acidification seascape and
its relationship to the performance of calcifying marine invertebrates: Laboratory experiments
on the development of urchin larvae framed by environmentally-relevant pCO2/pH. Journal of
Experimental Marine Biology and Ecology 400: 288-295.
Yu, P.C., Sewell, M.A., Matson, P.G., Rivest, E.B., Kapsenberg, L. and Hofmann, G.E. 2013. Growth
attenuation with developmental schedule progression in embryos and early larvae of Sterechinus
neumayeri raised under elevated CO2. PLOS ONE 8: e52448.
Cover photo of Tripneustes ventricosus (West Indian Sea Egg-top) and Echinometra viridis (Reef Urchin bottom) by Nick Hobgood as posted to Wikipedia under Creative Commons Attribution-ShareAlike 3.0
Unported license.
15
www.co2science.org
16