Introduction
The release of carbon dioxide (CO2) into the atmosphere by human
activities results in an increased flux of CO2 into a mildly alkaline
ocean, resulting in an increase in the concentration of inorganic carbon, and
a reduction in pH, carbonate ion concentration, and the capacity of seawater
to buffer changes in its chemistry. These changes are collectively known as
ocean acidification (Gattuso et al., 2014).
Investigations of the effect of ocean acidification on marine organisms and
ecosystems have a relatively short history. A wide range of sensitivities to
projected rates of ocean acidification exists within and across diverse
groups of organisms, with a trend for greater sensitivity in early life
stages (Kroeker et al., 2013). Several meta-analyses reveal a pattern of
positive and negative impacts (Gattuso et al., 2014) but key uncertainties
remain in our understanding of the impacts on organisms, life histories and
ecosystems.
The number of papers addressing biological responses to ocean acidification
has increased steeply in the past decade, from 18 papers per year in 2004 to
365 papers in 2014 (Gattuso and Hansson, 2011; OA-ICC bibliographic database,
www.tinyurl.com/oaicc-biblio). It is challenging to compare and
synthesize the results of these papers for two reasons. First, data are not
easily discoverable and accessible because they are either not archived or
archived in different data repositories in varying formats. Second, the
carbonate chemistry and ancillary data are often reported in different units
and scales, and calculated using different sets of constants, making the
carbonate chemistry across studies inconsistent. For example, it is crucial
to report the pH scale used, since pH reported on the free scale is about
0.11 to 0.12 units higher than on the total and seawater scales, respectively
(Zeebe and Wolf-Gladrow, 2001).
A compilation of ocean acidification biological response data was initiated
by the European Network of Excellence for Ocean Ecosystems Analysis
(EUR-OCEANS) and the European Project on Ocean Acidification (EPOCA) in 2008
(Nisumaa et al., 2010). This effort ended in 2012 when the EPOCA project came
to an end but was resumed in the framework of the Ocean Acidification
International Coordination Centre (OA-ICC) in 2013, in close collaboration
with Xiamen University and the world data centre PANGAEA. The goal of the
OA-ICC data compilation is to gather data on the biological response to ocean
acidification (carbonate chemistry, biogeochemical processes and ancillary
data) from published articles and to make them available in a coherent format
to the scientific community. As part of the effort, the carbonate system
variables are recalculated in a consistent way. Data from papers that report
at least two carbonate chemistry parameters, as well as temperature and
salinity, are included in the compilation. The data compilation has been very
well received by the ocean acidification community. It has been used in three
meta-analyses (Kroeker et al., 2010, 2013; Liu et al., 2010), a modelling
study (Muller and Nisbet, 2014) and cited in six other publications (Fiorini
et al., 2011; Hendriks and Duarte, 2010; Hoppe et al., 2012; Koeve and
Oschlies, 2012; Meyer and Riebesell, 2014; Rokitta, 2012). We report here on
the developments of this database 5 years since its first description by
Nisumaa et al. (2010). This update is timely, since 500 data sets from 439
papers (81 % of the total number included in the compilation) have been
archived since the publication of Nisumaa et al. (2010).
Data
The compilation process described in Nisumaa et al. (2010) was followed to
maintain consistency. Briefly, papers on the biological response to ocean
acidification were identified by searching the OA-ICC news stream
(http://news-oceanacidification-icc.org/) or through the OA-ICC
bibliographic database for older papers. Papers were excluded from the
compilation when they only used levels of partial pressure of carbon dioxide
(pCO2) or pH which are not consistent with present-day levels or future
scenarios. For example, data collected with a control condition with
pCO2 values below about 100 µatm or above
1700 µatm or pHT (on the total scale) values below
about 7.5 or above 8.5 were excluded unless they are environmentally relevant
at the study location. Data were requested from the authors by email. Data
were either provided by authors, or extracted from tables in the original
paper, or downloaded from other data repositories such as the Biological and
Chemical Oceanography Data Management Office (BCO-DMO), the British Oceanographic
Data Centre (BODC) and the Australian Antarctic Data Centre (AADC). All the data
sets archived in the framework of the OA-ICC (since 2013) as well as the
projects EPOCA/EUR-OCEANS (2008–2012) have been given the tag “Ocean
Acidification International Coordination Centre (OA-ICC)” in PANGAEA.
Between the beginning of this activity in 2008 and January 2015, 1026
relevant papers were identified. 581 data sets (over 4 000 000 data points)
were archived from 539 of these papers. Data from a paper can be archived as
several data sets (e.g. http://doi.pangaea.de/10.1594/PANGAEA.777725),
which explains why out of 539 papers, there were 581 data sets archived. Data
of the remaining 487 papers could not be added to the compilation for the
following reasons (Fig. 1): (1) less than two carbonate system parameters
were measured in 176 papers, preventing the recalculation of the carbonate
chemistry; (2) data from 295 papers could not be obtained from the authors;
and (3) data from 16 papers were lost by authors.
Cumulative number of papers for which data have been included in the
compilation (“archived”), papers for which data could not be obtained
(“not obtained”), papers which reported less than two carbonate system
parameters (“incomplete”) and papers for which the data have been lost
(“lost”).
![]()
The first papers having investigated a biological response to decreased pH
(e.g. Vernon, 1895) predate the definition of the pH scale by
Sørensen (1909) and are obviously not amenable to be included in the data
compilation. The earliest data included in the compilation were published in
1967 (Traganza, 1967). No data from the papers published during 1968–1993
could be archived because data were lost or could not be obtained. Data from
41 papers published during 1994 and 2006 were archived. The quantity of data
archived for a given year follows the increase in publication rate of
biological response papers, with data from 11 papers archived for 2007 to 110
papers for 2014. More than 90 % of the data archived in the compilation
come from papers published after 2007.
All the references of papers included in the data compilation have been
tagged with the keyword “OAICCdb” in the OA-ICC bibliographic database
(www.tinyurl.com/oaicc-biblio). The OA-ICC bibliographic database was
used to retrieve statistical information on the type of papers from which the
data archived originated. Keywords describing the geographical region, type
of organism and biological process studied, other factors manipulated, as
well as the country of affiliation of the first author were extracted from
the bibliographic database for statistical analysis. Results are presented as the
percentage of papers from which data were archived. Information on salinity,
temperature and carbonate chemistry data archived as part of the data
compilation were extracted from the PANGAEA data warehouse. The analyses of
these parameters were based on the percentage of data sets or count of data
points.
Geographical coverage
In the OA-ICC data compilation, the location of study sites indicates where
the studied organisms were collected or the location of the natural
communities investigated. The geographical location is not always clearly
indicated in the papers, and the bibliographic database does not provide
geographical information for experiments using organisms which have been
cultured for a long time in the laboratory or collected from commercial
hatcheries. The geographical areas which are best covered are the North
Atlantic Ocean, North Pacific Ocean, South Pacific Ocean and Mediterranean
Sea (33, 19, 17 and 10 %, respectively, of the papers indicating a
geographical location). The Arctic Ocean, Baltic Sea, Southern Ocean, Red
Sea, Indian Ocean and South Atlantic Ocean collectively represent only
21 % of the papers. In summary, most of the study sites to date have been
in the Northern Hemisphere, the number of studies from the Southern
Hemisphere and polar oceans are relatively low (Fig. 2). Data from 35 studies
performed in the Arctic Ocean were archived, 22 of them from the EPOCA
mesocosm experiment carried out in Kongsfjorden (Spitsbergen) in 2010
(Riebesell et al., 2013). There were data from 12 papers from the Southern
Ocean, all added after the publication of Nisumaa et al. (2010). This remains
a low number considering the fact that polar regions are particularly
vulnerable to ocean acidification (Orr et al., 2005; Steinacher et al.,
2009).
(a) Location of organisms and natural communities from
which data has been archived and (b) distribution of locations
according to latitude.
![]()
Taxonomic coverage
Phytoplankton (in 20 % of the papers in the data compilation) and corals
(18 %) are still the best represented taxonomic groups (Fig. 3), although
their percentages came down from, respectively, 39 and 29 % of the papers from which data were archived
before 2010 (Nisumaa et al., 2010). The relative number of papers studying
other taxonomic groups went up: molluscs (8 to 16 %), macroalgae (7 to
11 %), crustaceans (5 to 8 %), echinoderms (3 to 8 %) and fish (2
to 6 %). Sixty studies (11 %) investigated the response of a mix of
organisms or natural communities, while there were no such studies from which
data were archived before 2010, indicating a clear shift away from the study
of individual organisms to communities and ecosystems, as has been
recommended to close existing gaps in ocean acidification science (Riebesell
and Gattuso, 2015). This is important as data on competitive and trophic
interactions are key to better predict future impacts of ocean acidification.
The amount of papers concerning prokaryotes, protists, zooplankton and others
(annelids, virus etc.) are relatively low (less than 8 % for each
species).
Taxonomic coverage of the papers from which data have been included
in the OA-ICC data compilation, compared to those archived prior to 2010.
Categories marked with * were not present in Nisumaa et al. (2010).
![]()
Biological processes
The most studied biological processes are morphology, calcification and
growth, representing 33, 30 and 26 % of the papers from which data were
archived (Fig. 4). Physiology, photosynthesis, mortality, reproduction and
respiration are also well represented (13 to 23 %), followed by primary
production, performance, dissolution and nitrogen fixation. Other processes
such as community composition, abundance, adaption, nutrient uptake, toxicity
and bleaching are represented in 26 % of the papers from which data were
archived (see detail description of keywords in the user instructions of the
OA-ICC bibliographic database, www.tinyurl.com/oaicc-biblio). All
processes, except calcification and primary production, are better
represented today than they were before 2010, indicating that the initial
imbalance (of considerably more studies on calcification and primary
production than on other processes) has improved.
Biological processes reported in the papers from which data have
been included in the OA-ICC data compilation, compared to those archived
prior to 2010. Other processes studied in the papers from which data were
archived before 2010 comprise variables such as shell length, width and
linear extension of molluscs, bleaching, invasion, orientation, different
blood cell concentration, concentration in the tissues of organisms, rate of
nitrogen fixation (Nisumaa et al., 2010). The categories marked with *
were not present in Nisumaa et al. (2010) or their definition was different.
“Morphology” was included in “Other processes” in Nisumaa et al. (2010)
whereas it is considered as a distinct category in the present paper.
![]()
Multiple factors
There is a clear tendency towards more multifactorial studies after 2010.
Even though the majority of the compiled papers have only manipulated the
carbonate chemistry, their relative contribution in the data compilation
decreased from 81 (pre-2010) to 69 %. The main other factors studied in
addition to the carbonate system are temperature (14 % of papers),
nutrients (6 %) and light (5 %) (Fig. 5). Few papers manipulated
oxygen, metal or toxic compounds. Twenty papers have also reported combined
effect of changes in carbonate chemistry with two or three other factors. In
general, data from studies on multifactorial impact are still limited in the
data compilation. It is one of the major challenges faced by future ocean
acidification research (Riebesell and Gattuso, 2015).
Papers that have manipulated the carbonate chemistry alone and those
that have manipulated the carbonate chemistry as well as other variables. CC,
carbonate chemistry. The categories marked with * were not present in Nisumaa
et al. (2010).
![]()
Countries of first-author affiliation
Based on first-author affiliation, most of the data compiled are from
articles contributed by European countries (59 %; Fig. 6). Within Europe,
41 % of the papers were published by German scientists and 19 % by UK
scientists. The USA (18 %) and Australia (8 %) also contribute a lot
to the data compilation. There are still data from many papers which could
not be obtained from the authors from these two countries (87 and 49 papers,
respectively).
Countries of affiliation of first author of papers from which data
were archived and papers for which data could not be obtained.
![]()
Measured carbonate chemistry variables
A complete and consistent set of carbonate system variables was calculated by
the R package seacarb (Gattuso et al., 2015) as described by Nisumaa et
al. (2010), in order to provide coherent information on the
chemistry. The recalculated parameters were
archived together with the original ones and were flagged accordingly
(“Calculated using seacarb after Nisumaa et al., 2010” together with a
reference to the data curator responsible for the recalculation).
Total alkalinity (AT) is the carbonate chemistry variable that is
the most measured (79 % of the data sets; Fig. 7). The other variables
measured include pH (70 %), dissolved inorganic carbon (CT,
36 %) and the partial pressure of carbon dioxide (pCO2, 8 %).
Out of the 70 % data sets that measured pH, 38 % reported pH on the
National Bureau of Standard (NBS) scale (also referred to as the National
Institute of Standards and Technology, NIST, scale), 30 % on the
total scale, 1 % on the seawater scale (SWS) and 1 % on the free
scale (Fig. 7). Although the number of data sets with pH reported on the NBS
scale are still more than on the total scale, the ratio of them has been
decreased from 2.2 (pre-2010) to 1.2. The pH value on the total scale is 0.15
units lower than on the NBS/NIST scale and 0.01 units higher than on the
SWS scale (Dickson, 2010), which makes the direct comparison of experimental
results difficult. All other scales are converted to the total scale in this
compilation as recommended in the Guide to Best Practices in Ocean
Acidification Research and Data Reporting (Dickson, 2010).
Variables of the seawater carbonate system reported in the data
sets.
![]()
(a) Temperature, (b) salinity, (c)
pHT, (d) pCO2, (e) AT,
(f) CT, (g) aragonite saturation state,
(h) calcite saturation state and (i) carbonate ion coverage in the
compilation. The dashed vertical lines indicate the average open-ocean
surface values, during the Last Glacial Maximum (LGM), 1766, 2007 and 2100
(see the values in Table 1.1 of Gattuso and Hansson, 2011).
![]()
Temperature and salinity coverage
The temperature values reported range from -3 to 34 ∘C but most
temperature data are between 18 and 21 ∘C (Fig. 8a) and few values
are below 0 ∘C or above 30 ∘C. Salinity ranges from 4 to 65
with 60 % of the data points ranging between 32 and 36 (Fig. 8b). The
geographical distribution of the papers considered (Fig. 2) shows that the
study sites are distributed over all the oceans of the world, including the
high-salinity Red Sea and the low-salinity Baltic Sea. High-salinity lagoons
and low-salinity estuarine areas have also been studied, which can explain
the large range of salinity in the compilation. There are 36 data points with
salinity greater than 50 – they were derived from paper on brine algae
collected from sea ice in Antarctica (McMinn et al., 2014).
Carbonate chemistry variables coverage
pHT, pCO2, AT, CT, aragonite
(Ωa) and calcite (Ωc) saturation states and
carbonate ion (CO32-) data included in this compilation span the
range of the average open-ocean surface values from the Last Glacial Maximum
(LGM) to 2100 (Fig. 8). The largest number of data points are comprised
between pHT 7.65 to 7.95, pCO2 500 to 1000 µatm
and CT 2100 to 2200 µmol kg-1 (Fig. 8c, d, f).
This indicates that most studies used carbonate chemistries that are
environmentally relevant. Ambient pCO2 level is often used as the
control treatment, so many pHT,pCO2 and CT
data points are close to the present–day values (8.07, 384 µatm
and 2064 µmol kg-1). Few data points are close to the value
during LGM and 1766, because few studies used preindustrial and “glacial”
pCO2 level (respectively 267 and 180 µatm) as treatments.
Some data points are indicative of carbonate chemistry that are not
environmentally relevant (i.e. pCO2 below 150 µatm or above
2000 µatm, pHT below 7.35 or above 8.45). This is
because in some studies they not only used pCO2 and pHT
relevant to past or for future scenarios as treatments, but also used extreme
pCO2 and pHT as treatments. Since ATis unaffected
by the uptake of CO2, it has been recommended to keep it constant in
perturbation experiments, for example by bubbling seawater with CO2
enriched air (Gattuso and Lavigne, 2009). In the OA-ICC data compilation,
most of AT data points range from 2250 to
2350 µmol kg-1, which is close to the average present-day
open-ocean surface values (2325 µmol kg-1) (Fig. 8e).
However, some studies manipulated the carbonate chemistry by adding strong
acids and bases without restoring total alkalinity (see Gattuso et al.,
2010), which significantly altered AT. The number of this kind of
study has decreased since the publication of the Guide to Best Practices in
Ocean Acidification Research and Data Reporting (Cornwall and Hurd, 2016).
In addition, some low-AT data points were archived from studies
performed in low-salinity areas, such as the Baltic Sea and estuarine
areas. The concentration of CO32-, as well as Ωa
and Ωc exhibit similar distribution patterns, with most
number of data points close to their average value of surface seawater for
2100 (Fig. 8g, h, i).
Recommendations
As a new scientific field such as ocean acidification develops, the amount of
scientific data grows considerably and the need for data archiving greatly
increases to ensure that data are easily accessible for analysis and reuse.
Many journals, such as the Proceedings of the Royal Society B – Biological
Sciences, PLoS ONE and Nature, require or encourage authors to archive
data in public data repositories. Several data journals were launched to help
this process. For example, the present journal was launched by the European
Geosciences Union in 2008 and Scientific Data of the Nature publishing
group in 2014. Many funding agencies also have requirements on data
archiving. The European Research Council (ERC) mandate funded scientists to
deposit primary data in relevant databases as soon as possible after data
collection. In the United States, researchers seeking funding from the
National Science Foundation (NSF) are required to submit a data management
plan as a supplement to the grant application. Research projects such as the
European FP7 project EPOCA have provided guidelines on data reporting and
discussed the benefits of data archiving (Pesant et al., 2010). Although data
archiving is not only of benefit for the scientific community but also a
great way to advertise scientific work, get more citations (Piwowar et al.,
2007) and initiate new collaborations, it is a difficult task to collect data
from authors. It is a slow process and only data from 53 % of the
relevant papers could be included in the compilation. We therefore encourage
the international ocean acidification community to actively participate in
the data archiving effort.
Another challenge is the use of consistent variable names as papers sometimes
report the same variable with different names, for example “respiration”
and “oxygen consumption”. It is recommended to develop standard
vocabularies describing the variables. And the standard vocabularies should
be used in the metadata template to ensure effective data searching (Jiang et
al., 2015). At an expert meeting on the management of ocean acidification
biological response data organized by the Ocean Acidification International
Coordination Centre in 2014, ocean acidification scientists and data managers
from major data centres agreed to develop a list of the most common
biological parameters from ocean acidification studies (Hansson et al.,
2014). Journals are invited to make sure that variables of the carbonate
chemistry are reported in full and with the required level of detail (see
Supplement). Furthermore, some data have previously been published in PANGAEA
by data curators of other projects (e.g. the project “Biological Impacts of
Ocean Acidification”, BIOACID), or in other databases (e.g. the Biological
and Chemical Oceanography Data Management Office, British Oceanographic Data
Centre, Australian Antarctic Data Centre), which induced duplicates when they
were archived again for the OA-ICC data compilation with recalculated
carbonate chemistry data. To detect duplication, we recommend that the
community creates unique identification for data sets on the biological
response to ocean acidification. And it is hoped that all projects and
databases can define best practices for archiving ocean acidification data
and cooperate to avoid duplication. To this end and to meet the need for
easier and more effective access to ocean acidification data, data managers
of various institutions are planning to create a joint portal (“one-stop
shop”) for access to global ocean acidification data by linking different
data repositories (Garcia et al., 2015; Hansson et al., 2014). The Ocean
Acidification International Coordination Centre recently organized a
follow-up workshop to the last meeting in 2014 to work on the technical
details of the one-stop shop data portal.