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Study in nature: protecting the ocean delivers a comprehensive solution for climate, fishing and biodiversity.

Southern Line Islands

Photograph by Southern Line Islands

Groundbreaking global study is the first to map ocean areas that, if strongly protected, would help solve climate, food and biodiversity crises

London, UK (17 March 2021) —A new study published in the prestigious peer-reviewed scientific journal Nature today offers a combined solution to several of humanity’s most pressing challenges. It is the most comprehensive assessment to date of where strict ocean protection can contribute to a more abundant supply of healthy seafood and provide a cheap, natural solution to address climate change—in addition to protecting embattled species and habitats.

An international team of 26 authors identified specific areas that, if protected, would safeguard over 80% of the habitats for endangered marine species, and increase fishing catches by more than eight million metric tons. The study is also the first to quantify the potential release of carbon dioxide into the ocean from trawling, a widespread fishing practice—and finds that trawling is pumping hundreds of millions of tons of carbon dioxide into the ocean every year, a volume of emissions similar to those of aviation.

“Ocean life has been declining worldwide because of overfishing, habitat destruction and climate change. Yet only 7% of the ocean is currently under some kind of protection,” said Dr. Enric Sala, explorer in residence at the National Geographic Society and lead author of the study, Protecting the global ocean for biodiversity, food and climate .

“In this study, we’ve pioneered a new way to identify the places that—if strongly protected—will boost food production and safeguard marine life, all while reducing carbon emissions,” Dr. Sala said. “It’s clear that humanity and the economy will benefit from a healthier ocean. And we can realize those benefits quickly if countries work together to protect at least 30% of the ocean by 2030.”

To identify the priority areas, the authors—leading marine biologists, climate experts, and economists—analyzed the world’s unprotected ocean waters based on the degree to which they are threatened by human activities that can be reduced by marine protected areas (for example, overfishing and habitat destruction). They then developed an algorithm to identify those areas where protections would deliver the greatest benefits across the three complementary goals of biodiversity protection, seafood production and climate mitigation. They mapped these locations to create a practical “blueprint” that governments can use as they implement their commitments to protect nature.

The study does not provide a single map for ocean conservation, but it offers a first-in-kind framework for countries to decide which areas to protect depending on their national priorities. However, the analysis shows that 30% is the minimum amount of ocean that the world must protect in order to provide multiple benefits to humanity.

“There is no single best solution to save marine life and obtain these other benefits. The solution depends on what society—or a given country—cares about, and our study provides a new way to integrate these preferences and find effective conservation strategies,” said Dr. Juan S. Mayorga, a report co-author and a marine data scientist with the Environmental Market Solutions Lab at UC Santa Barbara and Pristine Seas at National Geographic Society.

The study comes ahead of the 15th Conference of the Parties to the United Nations Convention on Biological Diversity, which is expected to take place in Kunming, China in 2021. The meeting will bring together representatives of 190 countries to finalize an agreement to end the world’s biodiversity crisis. The goal of protecting 30% of the planet’s land and ocean by 2030 (the “30x30” target) is expected to be a pillar of the treaty. The study follows commitments by the United States, the United Kingdom, Canada, the European Commission and others to achieve this target on national and global scales.

Safeguarding Biodiversity

The report identifies highly diverse marine areas in which species and ecosystems face the greatest threats from human activities. Establishing marine protected areas (MPAs) with strict protection in those places would safeguard more than 80% of the ranges of endangered species, up from a current coverage of less than 2%.

The authors found that the priority locations are distributed throughout the ocean, with the vast majority of them contained within the 200-mile Exclusive Economic Zones of coastal nations.

The additional protection targets are located in the high seas—those waters governed by international law. These include the Mid-Atlantic Ridge (a massive underwater mountain range), the Mascarene Plateau in the Indian Ocean, the Nazca Ridge off the west coast of South America and the Southwest Indian Ridge, between Africa and Antarctica.

"Perhaps the most impressive and encouraging result is the enormous gain we can obtain for biodiversity conservation—if we carefully chose the location of strictly protected marine areas,” said Dr. David Mouillot, a report co-author and a professor at the Université de Montpellier in France. “One notable priority for conservation is Antarctica, which currently has little protection, but is projected to host many vulnerable species in a near future due to climate change."

Shoring up the Fishing Industry

The study finds that smartly placed marine protected areas (MPAs) that ban fishing would actually boost the production of fish—at a time when supplies of wild-caught fish are dwindling and demand is rising. In doing so, the study refutes a long-held view that ocean protection harms fisheries and opens up new opportunities to revive the industry just as it is suffering from a recession due to overfishing and the impacts of global warming.

“Some argue that closing areas to fishing hurts fishing interests. But the worst enemy of successful fisheries is overfishing—not protected areas,” Dr. Sala said.

The study finds that protecting the right places could increase the catch of seafood by over 8 million metric tons relative to business as usual.

“It’s simple: When overfishing and other damaging activities cease, marine life bounces back,” said Dr. Reniel Cabral, a report co-author and assistant researcher with the Bren School of Environmental Science & Management and Marine Science Institute at UC Santa Barbara. “After protections are put in place, the diversity and abundance of marine life increase over time, with measurable recovery occurring in as little as three years. Target species and large predators come back, and entire ecosystems are restored within MPAs. With time, the ocean can heal itself and again provide services to humankind.”

Soaking up Carbon

The study is the first to calculate the climate impacts of bottom trawling, a damaging fishing method used worldwide that drags heavy nets across the ocean floor. It finds that the amount of carbon dioxide released into the ocean from this practice is larger than most countries’ annual carbon emissions, and similar to annual carbon dioxide emissions from global aviation.

“The ocean floor is the world’s largest carbon storehouse. If we’re to succeed in stopping global warming, we must leave the carbon-rich seabed undisturbed. Yet every day, we are trawling the seafloor, depleting its biodiversity and mobilizing millennia-old carbon and thus exacerbating climate change. Our findings about the climate impacts of bottom trawling will make the activities on the ocean’s seabed hard to ignore in climate plans going forward,” said Dr. Trisha Atwood of Utah State University, a co-author of the paper.

The study finds that countries with the highest potential to contribute to climate change mitigation via protection of carbon stocks are those with large national waters and large industrial bottom trawl fisheries. It calculates that eliminating 90% of the present risk of carbon disturbance due to bottom trawling would require protecting only about 4% of the ocean , mostly within national waters.

Closing a Gap

The study’s range of findings helps to close a gap in our knowledge about the impacts of ocean conservation, which to date had been understudied relative to land-based conservation.

“The ocean covers 70% of the earth—yet, until now, its importance for solving the challenges of our time has been overlooked,” said Dr. Boris Worm, a study co-author and Killam Research Professor at Dalhousie University in Halifax, Nova Scotia. “Smart ocean protection will help to provide cheap natural climate solutions, make seafood more abundant and safeguard imperiled marine species—all at the same time. The benefits are clear. If we want to solve the three most pressing challenges of our century—biodiversity loss, climate change and food shortages —we must protect our ocean.”

Additional Quotes from Supporters and Report Co-Authors

Zac Goldsmith, British Minister for Pacific and the Environment, UK

Kristen Rechberger, Founder & CEO, Dynamic Planet

Dr. William Chueng, Canada Research Chair and Professor, The University of British Columbia, Principal Investigator, Changing Ocean Research Unit, The University of British Columbia

Dr. Jennifer McGowan, Global Science, The Nature Conservancy & Center for Biodiversity and Global Change, Yale University

Dr. Alan Friedlander, Chief Scientist, Pristine Seas, National Geographic Society at the Hawai'i Institute of Marine Biology, University of Hawai'i

Dr. Ben Halpern, Director of the National Center for Ecological Analysis and Synthesis (NCEAS), UCSB

Dr. Whitney Goodell, Marine Ecologist, Pristine Seas, National Geographic Society

Dr. Lance Morgan, President and CEO, Marine Conservation Institute

Dr. Darcy Bradley, Co-Director of the Ocean and Fisheries Program at the Environmental Market Solutions Lab, UCSB

The study, Protecting the global ocean for biodiversity, food and climate , answers the question of which places in the ocean should we protect for nature and people. The authors developed a novel framework to produce a global map of places that, if protected from fishing and other damaging activities, will produce multiple benefits to people: safeguarding marine life, boosting seafood production and reducing carbon emissions. Twenty-six scientists and economists contributed to the study.

Study’s Topline Facts

• Ocean life has been declining worldwide because of overfishing, habitat destruction and climate change. Yet only 7% of the ocean is currently under some kind of protection.
• A smart plan of ocean protection will contribute to more abundant seafood and provide a cheap, natural solution to help solve climate change, alongside economic benefits.
• Humanity and the economy would benefit from a healthier ocean. Quicker benefits occur when countries work together to protect at least 30% of the ocean.
• Substantial increases in ocean protection could achieve triple benefits, not only protecting biodiversity, but also boosting fisheries’ productivity and securing marine carbon stocks.

Study’s Topline Findings

• The study is the first to calculate that the practice of bottom trawling the ocean floor is responsible for one gigaton of carbon emissions on average annually. This is equivalent to all emissions from aviation worldwide. It is, furthermore, greater than the annual emissions of all countries except China, the U.S., India, Russia and Japan.
• The study reveals that protecting strategic ocean areas could produce an additional 8 million tons of seafood.
• The study reveals that protecting more of the ocean--as long as the protected areas are strategically located--would reap significant benefits for climate, food and biodiversity.

Priority Areas for Triple Wins

• If society were to value marine biodiversity and food provisioning equally, and established marine protected areas based on these two priorities, the best conservation strategy would protect 45% of the ocean, delivering 71% of the possible biodiversity benefits, 92% of the food provisioning benefits and 29% of the carbon benefits.
• If no value were assigned to biodiversity, protecting 29% of the ocean would secure 8.3 million tons of extra seafood and 27% of carbon benefits. It would also still secure 35% of biodiversity benefits.
• Global-scale prioritization helps focus attention and resources on places that yield the largest possible benefits.
• A globally coordinated expansion of marine protected areas (MPAs) could achieve 90% of the maximum possible biodiversity benefit with less than half as much area as a protection strategy based solely on national priorities.
• EEZs are areas of the global ocean within 200 nautical miles off the coast of maritime countries that claim sole rights to the resources found within them. ( Source )

Priority Areas for Climate

• Eliminating 90% of the present risk of carbon disturbance due to bottom trawling would require protecting 3.6% of the ocean, mostly within EEZs.
• Priority areas for carbon are where important carbon stocks coincide with high anthropogenic threats, including Europe’s Atlantic coastal areas and productive upwelling areas.

Countries with the highest potential to contribute to climate change mitigation via protection of carbon stocks are those with large EEZs and large industrial bottom trawl fisheries.

Priority Areas for Biodiversity

• Through protection of specific areas, the average protection of endangered species could be increased from 1.5% to 82% and critically endangered species from 1.1% to and 87%.
• the Antarctic Peninsula
• the Mid-Atlantic Ridge
• the Mascarene Plateau
• the Nazca Ridge
• the Southwest Indian Ridge
• Despite climate change, about 80% of today’s priority areas for biodiversity will still be essential in 2050. In the future, however, some cooler waters will be more important protection priorities, whereas warmer waters will likely be too stressed by climate change to shelter as much biodiversity as they currently do. Specifically, some temperate regions and parts of the Arctic would rank as higher priorities for biodiversity conservation by 2050, whereas large areas in the high seas between the tropics and areas in the Southern Hemisphere would decrease in priority.

Priority Areas for Food Provision

• If we only cared about increasing the supply of seafood, strategically placed MPAs covering 28% of the ocean could increase food provisioning by 8.3 million metric tons.

The Campaign for Nature works with scientists, Indigenous Peoples, and a growing coalition of over 100 conservation organizations around the world who are calling on policymakers to commit to clear and ambitious targets to be agreed upon at the 15th Conference of the Parties to the Convention on Biological Diversity in Kunming, China in 2021 to protect at least 30% of the planet by 2030 and working with Indigenous leaders to ensure full respect for Indigenous rights.

Media Contact

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• A-Z Publications

Annual Review of Environment and Resources

Volume 45, 2020, review article, open access, the impacts of ocean acidification on marine ecosystems and reliant human communities.

• Scott C. Doney 1 , D. Shallin Busch 2 , Sarah R. Cooley 3 , and Kristy J. Kroeker 4
• View Affiliations Hide Affiliations Affiliations: 1 Department of Environmental Sciences, University of Virginia, Charlottesville, Virginia 22904, USA; email: [email protected] 2 Ocean Acidification Program and Conservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, Washington 98112, USA; email: [email protected] 3 Ocean Conservancy, Washington, DC 20036, USA; email: [email protected] 4 Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, California 95064, USA; email: [email protected]
• Vol. 45:83-112 (Volume publication date October 2020) https://doi.org/10.1146/annurev-environ-012320-083019
• First published as a Review in Advance on June 24, 2020
• Copyright © 2020 by Annual Reviews. This work is licensed under a Creative Commons Attribution 4.0 International License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. See credit lines of images or other third party material in this article for license information.

Rising atmospheric carbon dioxide (CO 2 ) levels, from fossil fuel combustion and deforestation, along with agriculture and land-use practices are causing wholesale increases in seawater CO 2 and inorganic carbon levels; reductions in pH; and alterations in acid-base chemistry of estuarine, coastal, and surface open-ocean waters. On the basis of laboratory experiments and field studies of naturally elevated CO 2 marine environments, widespread biological impacts of human-driven ocean acidification have been posited, ranging from changes in organism physiology and population dynamics to altered communities and ecosystems. Acidification, in conjunction with other climate change–related environmental stresses, particularly under future climate change and further elevated atmospheric CO 2 levels, potentially puts at risk many of the valuable ecosystem services that the ocean provides to society, such as fisheries, aquaculture, and shoreline protection. Thisreview emphasizes both current scientific understanding and knowledge gaps, highlighting directions for future research and recognizing the information needs of policymakers and stakeholders.

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From Darwin to the Census of Marine Life: Marine Biology as Big Science

* E-mail: [email protected]

Affiliation Centre for the History of Science, Technology and Medicine, University of Manchester, Manchester, United Kingdom

• Niki Vermeulen

• Published: January 14, 2013
• https://doi.org/10.1371/journal.pone.0054284
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With the development of the Human Genome Project, a heated debate emerged on biology becoming ‘big science’. However, biology already has a long tradition of collaboration, as natural historians were part of the first collective scientific efforts: exploring the variety of life on earth. Such mappings of life still continue today, and if field biology is gradually becoming an important subject of studies into big science, research into life in the world's oceans is not taken into account yet. This paper therefore explores marine biology as big science, presenting the historical development of marine research towards the international ‘Census of Marine Life’ (CoML) making an inventory of life in the world's oceans. Discussing various aspects of collaboration – including size, internationalisation, research practice, technological developments, application, and public communication – I will ask if CoML still resembles traditional collaborations to collect life. While showing both continuity and change, I will argue that marine biology is a form of natural history: a specific way of working together in biology that has transformed substantially in interaction with recent developments in the life sciences and society. As a result, the paper does not only give an overview of transformations towards large scale research in marine biology, but also shines a new light on big biology, suggesting new ways to deepen the understanding of collaboration in the life sciences by distinguishing between different ‘collective ways of knowing’.

Citation: Vermeulen N (2013) From Darwin to the Census of Marine Life: Marine Biology as Big Science. PLoS ONE 8(1): e54284. https://doi.org/10.1371/journal.pone.0054284

Editor: Mande Holford, The City University of New York-Graduate Center, United States of America

Received: September 16, 2012; Accepted: December 10, 2012; Published: January 14, 2013

Copyright: © 2013 Vermeulen. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: The Wellcome Trust provided the funds to make this publication open-access. No other external funding sources. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The author has declared that no competing interests exist.

Introduction

While the discovery of space is well under way and almost every piece of land in the world has been discovered and mapped, not much is known about the world's oceans that cover about 70% of the earth's surface. Especially life in the depth of the oceans and invisible life such as micro-organisms are still a big mystery. This inspired the ‘Census of Marine Life’ (CoML), a large-scale international research project that took place during the first decade of the new millennium. The collaboration did not only reveal micro-organisms, but also aimed to catalogue all the animals in the world's oceans, including life in the deep-sea “to assess and explain the diversity, distribution, and abundance of marine life in the oceans – past, present, and future” [1] . This means that the Census of Marine Life is part of a natural history tradition in which collaboration is necessary for the collection of research materials that are globally dispersed [2] – [3] . While the Human Genome Project (HGP) is often presented as the first large-scale research project in the life sciences, natural history shows that scientific collaboration is hardly new to biology. It is found already in the alliance between science and exploration that set out to map the world and collect and describe its diverse forms of life [4] . However, studies of scientific collaboration pay little attention to these collaborations that collect, identify and catalogue life. If field biology is gradually becoming an important subject of studies into big science [5] – [9] research into the world's oceans is not taken into account yet. This paper will therefore explore large-scale research efforts in marine biology further. Does CoML still resemble traditional collaborations to collect life, or have developments in biology research and recent changes in the relation between science and society transformed marine biology research?

Presenting marine biology as big science, the paper will start with an introduction into big science and the discussion on big biology. After an overview of the historical development of marine biology, it will present the Census of Marine Life as a contemporary example of such collaboration, showing transformations in marine biology. By discussing various aspects of collaboration, including size and diversity, internationalisation, research practice, technological developments, the application of research, and public communication, the paper shows how the exploration of life in the oceans started hundreds of years ago with relatively small forms of collaboration that developed over time, increasing in scale and scope while also transforming research practice. Contemporary developments in science and society have become integrated in the traditional natural history style of research, transforming the ways in which life is measured, mapped and modeled. By analyzing marine biology as an example of big science, this paper will not only give an overview of transformations in marine biology as a type of natural history research, but also shine a new light on ‘big biology’ and the ways in which large-scale collaboration in biology can be understood.

Materials and Methods

The argument in this paper is based on an interdisciplinary study of scientific collaboration in biology, combining historical, philosophical and sociological perspectives [10] , [11] . Next to an extensive analysis of existing theory on scientific collaboration, empirical research covered various contemporary large-scale collaborations in the life sciences, including the Census of Marine Life. This paper is therefore not a direct result of the History of Marine Animal Populations that is part of CoML and has as its main concern the reconstruction of human-nature relations over time and the exploration of historical exploitations patterns in marine ecosystems. In contrast, the paper shows the historical development of research into marine biology. Nevertheless, these two subjects are indirectly related, as research into marine life has been influenced by human-nature relations and has also played an important role in shaping those relations. In order to analyze the ways in which scientific collaboration in marine biology has transformed over time, the paper draws on conceptual analysis of the ‘big science’ concept and an analysis of literature on the development of ocean research and marine biology. To study CoML as a contemporary collaboration in marine biology, I used qualitative methods, including document analysis, interviews with key actors in the project, and attendance of CoML meetings in the period 2005–2010.

Analysis and Results

Big science.

The Census of Marine Life is part of a broader development towards large-scale projects in biology, also called ‘big biology [12] . The origin of the term ‘big science’ lies in the United States where physicist Alvin Weinberg coined the term in 1961 [13] , while the concept was further developed by historian of science Derek de Solla Price in his book Little Science, Big Science [14] . Their work is part of a pile of books with the term ‘big’ in the title that all address growth as a distinctive phenomenon of modern society, covering big business, big government, big democracy, big school, big machine, big foundations and big cities [15] – [22] . Like all these ‘big books’, Weinberg and De Solla Price write about increasing dimensions full of wonder and admiration, but at the same time evaluate them critically. Growth is described as part of progress and an inevitable exponent of modern industrial society, while it is also seen as a source of problems. Thereby the books on bigness breath the ambivalence of the modern condition: “To be modern is to find ourselves in an environment that promises us adventure, power, joy, growth, transformation of big ourselves and the world – and, at the same time, that threatens to destroy everything we have, everything we know, everything we are” [23] .

Accordingly, from its emergence the concept of big science has an ambivalent understanding of growth that is characteristic for the modern condition and which is still very much visible in the two opposing views on big science in the debate on big biology, that emerged together with the Human Genome Project and subsequent increases in the organization of biology. Proponents present large-scale science as the new and more effective way to perform research nowadays: “scientific leaders agree that collaborative projects can produce results that would be impossible for specialized individuals working alone to achieve” [24] . In contrast, according to opponents big biology industrializes, bureaucratizes and politicizes research and dilutes creativity. To illustrate, genome sequencing was portrayed as “massive, goal-driven and mind-numbingly dull” [25] . Molecular biologist Sydney Brenner even joked that sequencing is so boring it should be done by prisoners: “the more heinous the crime, the bigger the chromosome they would have to decipher” [26] . In these discussions, the term big science provided the discussants with a strong rhetorical sword, but they never explicitly reflected on the concept itself or the specific ways in which biology became big science.

Besides being normative, big science also developed empirical significance, starting with De Solla Price's book that studies transformation in science. Originally a physicist, Price became interested in the history of science, and the annual expansion of the Philosophical Transactions of the Royal Society triggered his fascination for what he later would call big science: “the piles made a fine exponential curve against the wall, I (…) discovered that exponential growth, at an amazingly fast rate, was apparently universal and remarkably longlived” [27] . This stimulated his work on the quantitative measurement of scientific development and scientometrics [28] . In addition to big science being a quantitative empirical phenomenon, the concept is connected to qualitative studies of scientific transformation. Against the background of the development of Science and Technology Studies, big science has been used to look into historic and contemporary practices of research collaboration. Detailed case studies of different forms of big science in fields as diverse as astronomy, ecology, physics and space research enriched the empirical understanding of big science [29] . The emergence of large-scale research complexes is perceived as a broader trend and common features are not only found in growing numbers but also in large, expensive instruments, industrialisation, centralisation, multi-disciplinary collaboration, institutionalisation, science-government relations, cooperation with industry, and internationalization. Themes that also feature prominently in more recent studies of scientific collaboration [12] , [29] , [30] .

As a result, the big science concept should be seen as a historic concept that was formed in the 1960s to reflect on increasing dimensions in science, while acquiring different meanings over time: the big science concept has an empirical as well as an evaluative side. Moreover, when looking at big science empirically, a division can be made between a quantitative and a qualitative perspective and when using the concept to evaluate, positive as well as negative views on big science can be distinguished. Remarkably, discussions on big biology do not reflect on these different meanings, nor use the empirical side of the concept to investigate what kind of transformations actually take place in biology. Moreover, this disconnection results into an exclusive concern with the attributes of bigness, drawing attention away from “the more significant and interesting question of how science becomes larger” [31] . It is this process of making science big that I have called the ‘supersizing of science’ and the Census of Marine Life is an excellent example of the expansion of marine biology research.

Marine biology as big science

Although particle physics and space research are identified as typical forms of big science with gravitating activity around large-scale technology, it is biology that has the longest tradition in scientific collaboration all be it on a smaller scale. Natural historians were part of the first forms of scientific collaboration, described as the ‘grand alliance’ between science and exploration in the 17th century. Traditionally, natural history research took place in the context of the Renaissance, figuring trading nations, empire building and the establishment of scientific societies and national museums and the most important reason for cooperation in biology was the dispersed character of biological material [2] , [3] . Natural historians joined expeditions exploring the unknown world in order to describe, collect and catalogue new species, accumulating facts about plants and animals. In 1600 only around 6000 plant species of plants were known; by 1700 botanists had added discovered 12,000 new species, with similar accumulations in zoology. This advanced classificatory schemes– leading to Linnaeus's Systema Naturae [32] and the evolutionary theories of Lamarck [33] and Darwin [34] – but also changed in significant manners the ways in which biologists related and communicated with one another and acquired their research materials; infrastructural developments in transportation and communication technologies were crucial for these first forms of collaboration.

The great scientific voyages of the 18th and 19th centuries – including Charles Darwin's famous journey aboard the HMS Beagle – only explored species near the surface of the ocean, because they had neither access to nor knowledge of the deep oceans. For a long time it was thought that life could only be found there and at the ocean surface, as the absence of light, low temperatures and the density of water in the deep ocean was assumed to prevent life. However, these ideas slowly changed with the development of technologies that made the deep ocean visible [35] – [37] . At first, scientists began to investigate the depth of oceans. Sound to measure depth was first ventured by the Swiss mathematician Colladon in the Lake of Geneva, using a church bell and an ear trumpet. In 1838 this method was transferred to the ocean using explosions. In 1853 this developed into the so-called ‘soundingline of Brooke’ which was employed by the US Navy Depot of Charts and Instruments to map the North Atlantic Ocean. Thereby they discovered the ‘telegraphic plateau’ between Newfoundland and Ireland, which would be used by the Atlantic Telegraphy Company for the first trans-oceanic cable in 1858. In the 1870s the crew of the converted warship Challenger – known as the mothership of oceanography – discovered the Mid-Atlantic Ridge. As a result, scientists slowly began to realise that the oceanfloor had similar characteristics as the earth's surface, and in 1904 the newly established International Hydrographic Bureau published the first bathymetric standardised chart of the world ocean, based on 18400 soundings.

In the 20th century, ocean research gradually professionalized [38] – [40] . Next to telegraphy, shipping traffic, and the Titanic disaster, the World Wars and the following Cold War were important incentives to develop new technologies to survey the oceans and ocean research became institutionalised. To illustrate, the in 1930 founded American Woods Hole Oceanographic Institution (WHOI) played an important role in the development of oceanography. The history of the research vessels used by the institute gives a nice overview of the evolution of research vessels from traditional small sail and steamer ships to the modern big research vessels that are used today [41] . From the 1960s onwards, marine science increasingly became an academic endeavour and the 1970s were even pronounced to be the decade of ocean research. As a follow-up of the International Geophysical Year, the 1970s were arranged to be the International Decade of Ocean Exploration (1971–1980), aimed to scale-up ocean research to an international level [42] .

As marine biology developed in close interaction with these more general explorations of the oceans, actual observations of life in the deep-sea are of fairly recent date [35] , [36] , [38] . In the 19th century the Irishman Forbes developed and professionalized the art of dredging in order to explore life in the deep. Later, scientists from the Woods Hole Institute combined a dredge and trawl into a so-called ‘epibenthic sled’, used for bringing the diversity of life in the deep oceans to the surface. In the course of the 20th century, scientists have increasingly gained access to the deep ocean, facilitating direct observation of life in the deep-sea. The development of the ‘bathysphere’ – a kind of underwater balloon – in the 1930s enabled the first observations of life. Later, in the 1960s, the ‘bathyscape’ – a kind of underwater zeppelin for two men – descended to the Challenger Deep of the Mariana Trench (at about 11 kilometres the deepest known spot in the oceans). They spend 20 minutes there and saw a fish, which indicated that even in the deepest ocean life is possible. The construction of the submersible with robot-arms ‘Alvin’, in 1964, gave researchers even better access to the depths of the ocean, as did the development of deep-sea cameras. In short, the investigation of oceanlife developed through interaction between scientific curiosity, societal exploitation of the sea and technological developments.

Investigations into the oceans and their living creatures is big science avant la lettre. “Marine studies in general have a very early history in collaboration: it is essentially big science” [43] . In marine biology, large-scale collaboration is not only stimulated through the globally dispersed nature of the research material but also through a multi-disciplinary approach: “The multidisciplinary character of problems asks for collaboration between for example biologists, physicists and chemists” [44] . Moreover, technology is a reason to collaborate as costs are high: “The instruments of marine science can be compared to the large and expensive instruments that are used in physics and astronomy, like huge telescopes and cyclotrons (…) for instance a research vessel costs about $60 million” [45] . However, attention and funds for this branch of science is still very small compared to, for instance, research into space [46] [45] . Nevertheless, today's debates on climate change and biodiversity have granted more prominence to ocean research and efforts such as the Census of Marine Life.

The Census of Marine Life

Taking the collection work of Charles Darwin and his fellow natural historians some big steps further, the Census of Marine Life aimed to make an inventory of all animal life in the oceans –from the ocean shores to the deep-sea and from the poles to the Caribbean. CoML was put together at the end of the 20 th century, lasted 10 years (2000–2010), and involved 2,700 scientists, 80+ nations, 540 expeditions, US$ 650 million [47] , [48] . It resulted in 2,600+ scientific publications, 6,000+ potential new species, 30 million species records and results are still being produced. The story goes that the project started during holidays at the seaside, with two men - Fred Grassle, a professor in benthic ecology at Rutgers University, and Jesse Ausubel, programme officer with the Alfred P. Sloan Foundation and professor in human ecology at the Rockefeller University in New York - meeting over a beer and discussing the possibilities to put more focus on biodiversity. They came up with the idea of counting the ocean's fishes and started to set-up the project that later became known as the Census, in interaction with the marine biology community and with the support of funding for coordination of research from the Sloan Foundation. CoML comprised seventeen global projects. First of all, fourteen field projects mapped current life in the oceans, varying from the deep-sea to the shores and from Antarctic life to coral reefs. The results were catalogued into a database by an overarching project. Finally, two projects studied respectively the past and present of life in the oceans: the History of Marine Animal Population and the Future of Marine Animal Populations. As a result, the Census existed of a patchwork of projects that was held together by a central governance structure: a Scientific Steering Committee with a secretariat, as well as regional nodes.

With its objective to catalogue life in the oceans, the Census of Marine Life could be defined as a form of contemporary natural history collaboration. The project especially enabled the making of connections, thereby transforming the life of the scientist involved: “The programme is about the connections (…) The Census is only possible if you are a community and you share the same language and the same world” [44] . Connections made within the Census were geographical – as it brought researchers from diverse countries together – as well as epistemological, as it brought disciplines together in a multi-disciplinary effort, and fostered diverse research questions and approaches. Connections were made on the governance level and in the various research parts of the Census. Although the scientists within a project often already knew each other, the collaboration developed the contacts:

You are able to work with the same samples, with the same goals. For example, we work together with a large group on zooplankton and we worked together on the cruise to gather the samples and now we are also going to work together in the lab to analyse the samples. In this way you can sort things out together and discuss strange things you encounter. (…) in this way the relationships become clearer, you have more insight in the connections. [49]

In other words, within the Census colleagues became collaborators, enlarging the knowledge of biodiversity within the oceans ecosystems. However, when comparing it with earlier forms of collaboration to collect life, it was also larger, profiting from scientific and technological advancement, transforming research practice and results (e.g. virtual database, modelling), while emphasizing application and public communication.

Although natural history has been a collaborative effort from its start, the Census of Marine Life had unprecedented global ambitions, covering all the world's oceans as well as the diverse areas within these oceans, within the 14 field projects. While the Census started out as an American initiative, it became an international endeavor with over eighty countries participating. First, it stimulated cooperation between the United States and Europe: “This kind of collaboration has great additional value as people in Europe and the US have different specializations that we can now bring together which gives us new insights” [49] . And after covering the East and West Atlantic, the Census soon spread towards other regions as well: “Many countries, including India and China, have strong research programmes in marine biodiversity, which should enhance the longer term focus on Census related issues” [43] . Global expansion was supported by the creation of regional and national nodes in amongst others Australia, Canada, the Caribbean, China, Europe and the Indian Ocean. And next to space, time was an important dimension in the expansion of CoML. While the project itself took 10 years, its research intended to cover past, present and future, explicated in the three overarching research questions: what lived in the oceans, what lives in the oceans and what will live in the oceans? For answering such broad and complex questions a global collaborative effort was a requirement. And although the project's goal of counting and mapping all animal life in the oceans was clearly not reachable within one single decade, the final meeting of the Census in October 2010 presented many findings as well as some plans to extend the project into the next decade.

Technology development.

Building on the history of ocean research, the Census made use of the most advanced technologies, and developed them within special technology working groups. Technologies were related to various research practices and stages. For transportation the research vessel was the most important technology, but also, helicopters and planes were used, for instance to access remote areas or to study whales. For underwater exploration manned submersibles, remotely operated vehicles (ROV's), autonomous underwater vehicles (AUV's) and Deep-Towed Vehicles (DTV's) were used. Next to technologies for transport, the Census employed technologies for observing, counting, collecting and studying movement: acoustic technologies (such as sonar and echo) and optical technologies (e.g. cameras, videos, lasers, satellites, microscope). The collection of samples took place with the help of (traditional) fishnets, trawlers, sledges, bottles, traps and by hand. Finally, the movements of fish was studied with the help of fishnets, satellites, sonar, echo and the tagging of fish. For example, the website of the TOPP project (Tagging of Pacific Predators) followed the movements of tagged predators such as sharks, turtles and elephant seals. Within the research projects scientists experimented with the use of these various technologies: “It is really good that attention is given to technology. On the one hand attention is given to technologies and expertise that is already available within the project, and on the other hand new opportunities are explored” [49] . Technologies enabled new visions of life and transformed research configurations, through the transformation of the spatiality of the research situation, the place of action and the area of attention.

Reinventing taxonomy.

The transformation of research practices in interaction with developments in technology could also be seen in the case of taxonomy: the identification of species that is fundamental to natural history. Although it was a crucial practice within the Census and biology at large, it was and still is extremely difficult to find funding for taxonomic research. Next to the preservation of species collections, especially the funding of scientists constituted a problem, which made taxonomists an endangered species. As a result the Census focused on the development of technologies to determine species: “They explore if there are other possibilities than the traditional labour intensive determination using a microscope” [49] . Especially, the integration of genetic technologies within taxonomic practices was an important issue and the Census set up a DNA working group, which gave birth to the barcoding of life initiative. In analogy with using barcodes to identify manufactured goods, the DNA barcode initiative wanted to enable the identification of species by sequencing a uniform target gene, either in the laboratory or through a kit that could be used in the field [50] , [51] . On the one hand the use of DNA to identify species enhanced taxonomic practice, and enabled the identification of species that could not be identified by traditional taxonomic methods, such as micro-organisms that account for more then 90 percent of oceanic biomass, or creatures from the deep sea which are often damaged as a result of changes in pressure. Moreover, genetic information played an important role in determining the relation between different species, and enabled the identification of new species and the relationship between species. On the other hand the use of genetic technologies did not really replace old-fashioned taxonomy, as the making of the barcode system required taxonomic expertise and the barcoding did not always work in practice: “For some fishes it works and for others it doesn't” [44] . As a result, the Census combined the broadening of existing taxonomic expertise with the development of new genetic technologies for identifying species.

Building a new information infrastructure.

In natural history collaboration, data about species are always the main result of research. The way in which these data are assembled, standardised, integrated and stored is crucial, not only for the research practice, but also for the future outlook on life [52] , [53] . Therefore, developments in information technologies transform the way in which data are stored, creating new memory practices. This also became apparent in the Census of Marine Life that has developed its own database called OBIS, which stands for Ocean Biogeographic Information System [54] . “OBIS lets you trawl 12 marine databases for collection records” [55] and has continuously expanded. OBIS performed an important role in the formation of the collaboration, and it collected the various research results, making them freely available on the internet. The socio-technical connections that made up OBIS integrated the diverse research projects and underpinned the collaboration that investigated life in the oceans. More specifically, the database combined two types of information: information on living organisms (taxonomic databases) and geographical information (GIS), displaying where species have been found. It is important to note that data sharing has been an essential part of OBIS from its start and the open-access database has become the lasting legacy of CoML provided that it will be continuously maintained and updated. In addition, CoML stimulated open-access publishing, encouraging researchers to publish in the journals PLoS Biology and PLoS One, creating CoML Collections related to results from the diverse projects ( http://www.ploscollections.org ) and collaborating towards an open-access Biodiversity Hub ( http://hubs.plos.org/web/biodiversity ). As such CoML was one of the first big science projects that emphasized the importance of global access to research data and results, setting an example to the wider scientific community to commit to open-access publishing.

Tracing the past and modelling the future.

While natural history research has always served as a basis for learning and theorising about the development of life, this mainly concerned the evolution of life. In contrast, CoML aimed to use historic and contemporary data to explicitly learn about the future of ocean life. First, the History of Animal Populations project reconstructed direct human-nature relations over time, for instance through historic records of fish and the study of fish availability and prices on old restaurant menus. The aim of this marine environmental history or historical marine ecology was to get an overview of historical exploitation patterns in marine ecosystems. Through combining data on ocean life in the past with contemporary research data, CoML explicitly aimed to learn about the future. Therefore the Future of Marine Animals Project (FMAP) developed models to interpret historical data, designed field studies, synthesized data and made predictions about the oceans of the future. FMAP produced some interesting results, most notably a prominent publication in Science [56] on the downward trend in the diversity of fish in the open ocean due to fishery activities. By comparing information on the number of tuna and billfish caught on a standard longline with 1000 hooks from 1952 to 1999, the authors put together an overview of the decrease of fish in the open ocean, resulting in a striking visualization of a downward trend of 50%, coinciding with the emergence of large-scale commercial fishing. As this has serious consequences for marine biodiversity at large, the study resulted in global news coverage and gave rise to policy discussions. This is not to deny that Census scientists were struggling to fulfill their promise to predict the future of ocean life. The modelling of life in the oceans proved to be a real challenge, because the modeling efforts were relatively small and there was also not a proper picture of past and present ocean life in order to design a future model. Moreover, the Census scientists experienced that models cannot handle the complexity and unpredictability of ecosystems, as models can only contain a limited number of state variables, while ecosystems contain enormous amounts of species.

Application of research.

While the application of research is not the primary goal of natural history research, the Census scientists experienced a clear shift in research policy from fundamental towards applied research. Although the Sloan Foundation recognized the value of fundamental research and supported it, other funding sources simply did not fund this kind of research and required applications. The relevancy of marine biology has from the 1970s onwards been found in environmental problems developing from pollution to climate change and biodiversity. A good example of an environmental application is the use of newly discovered marine microbes to solve ‘challenges’ concerning energy production, global climate change mitigation and environmental cleanup. In addition, research within marine life had some concrete (industrial) applications, such as technology development in the areas of information technology, the tracking of organisms, satellite connections, online observatories and genomics. In analogy with space research, marine science also helped to develop new materials, for instance isolation material, and underwater circumstances provided knowledge about what happens with life at low levels of oxygen. Finally, funding organisations often stimulated collaboration with industry in order to apply research. For marine science, this involved an array of companies and business activities, ranging from aquaculture or fisheries to instrument makers, and the pharmaceutical and energy industry. However, the most important application of CoML might well be found in its policy advice. Although not anticipated by the scientists from its start, the Census has contributed to the development of policies related to marine observation, planning and protection [48] .

Showing the public.

Since the emergence of (public) aquariums, Jules Verne's Vingt mille lieues sous les mers [57] and the movies of Jacques Cousteau, the underwater world has been a public attraction. In line with this tradition, the Census provided a new impetus to the public's awareness of life in the oceans, and thereby it also reflected the current trend towards the embedding of science in society. “The oceans, like the heavens, offer a preferred route to increasing public understanding of the world in which we live, and of science” [58] . According to the Sloan Foundation researchers should share what they do with the society: “Sloan does not think of ‘public relations’. Sloan seeks to advance both the scientists' understanding of the public and the public understanding of science” [59] . Consequently, the international secretariat of the Census developed a communication strategy – which resulted in frequent worldwide newspaper coverage – and all projects were required to pay attention to interaction with the public. Also the web was an important part of CoML, with a main portal giving general information on the Census and an introduction to its different components while each project had its own website with detailed information on research plans, activities and outputs. On top of making public communication daily business, various special initiatives were developed, including several books on life in the oceans, a travelling exhibition called ‘Deeper than Light’, and an Ocean movie directed by Jacques Perrin who made successful documentaries on monkeys, insects and birds before. Last but not least, the Census projects and scientists were involved in educational activities, making children aware of the importance of our living environment and stimulating them to choose a career in science. As a result, CoML has build on the public fascination for ocean life and expanded it further using both traditional and more modern forms of public communication.

Conclusions

New natural history.

According to sociologist of science Arie Rip [60] the ‘new natural sciences’ are still measuring, mapping and modelling the world, as the natural sciences always did, but now in a more sophisticated way, due to developments in information and communication technologies. In line with this argument, my analysis of transformations in marine biology collaborations – which can be seen as a form of natural history – has articulated issues of continuity and change. Continuity can be seen in measuring and mapping which was also the very design of the Census project. For one thing, the scientists named their project ‘Census’: it was about counting and mapping what populates the sea. And during one of the initial meetings of the Census, the project was presented as part of the exploration of the world: “The age of discovery is not over. Indeed, the voyages of discovery open to Charles Darwin, Captain Cook, and the explorers of Linnaeus' century are very much open to the voyagers of 2000 and beyond” [61] . However, the Census also showed how research has changed substantively, not only through ICT but in interaction with recent scientific, technological and societal developments. Together, these transformations reinvented marine biology as a form of natural history, making up what we may call new natural history.

To start, the scale and scope of marine biology is becoming ever larger. With the participation of more than 80 countries CoML aimed to cover all the worlds' oceans, broadening the scope of research geographically. As a result, marine biology has basically become a global effort. Next to this globalization, taxonomic research – a vital part of natural history – has transformed fundamentally. Where taxonomists traditionally used morphology to identify species, now a shift took place towards genetic identification, broadening the biological scope of the research, including the animals of the deep-sea and the world of micro-organisms. In addition, the integration and contextualisation of knowledge can be observed. Although identification and cataloguing of species was central, this was increasingly presented as a starting point for the creation of new knowledge through the integration of data. The inventory of ocean life was a tool that could be used in further research on the interaction between species and their environment: “We have to start with an inventory of good quality and you may then really focus on questions to explain relationships within biology” [44] . This increasing focus on ecosystems meant the integration of information about life and geography, which became visible in OBIS and modelling initiatives that contextualised knowledge about life and looked at its development over time. Finally, technological development and new relationships between science and society transformed research practices. The examination of the Census showed how the development of new technologies was part of changing research configurations that brought new visions of life. This could not only be seen in the transformation of taxonomic practices through genetic technologies, but also in the widening of observation through satellite technology and the building of the new information infrastructure OBIS, creating a new outlook on life in the oceans. Developments in the relationship between science and society were reflected in increasing attention to public communication and the application of marine research.

Moreover, the analysis of the Census showed how new natural history comes with its own particular problems. While the process that Rip [60] calls ‘sophistication’ implies that measuring, mapping and modelling practices are now more advanced and maybe even more effective, CoML put some major problems in today's marine biology forward. For instance, the use of genomics technologies for identifying species did not seem to solve the shortage of taxonomists and gave rise to controversies about ‘proper’ taxonomy. In addition, tensions between an international research scope and national funding structures were an important bottleneck for collaborative research, as was true of the lack of international governance structures geared to stimulating and regulating international ocean research. This caused that the limits of growth in marine biology collaborations became apparent: not all countries participated and not all species were catalogued. And finally, the Census of Marine Life struggled with the integration of all the available research material and the building of models. However, despite of relatively short-term funding cycles, the project also underscored the remarkable resilience of big science [62] , as it seeks to extend itself into the future to eventually accomplish its goals.

Reflections

In their characterisation of the big science concept, Capshew and Rader [31] present growth as the most important aspect of science: “the growth of science is perhaps its most notable historical characteristic, whether considered in terms of scope, scale, complexity, or impact”. While the discussions on big biology emphasized growth in the context of the Human Genome Project, this analysis of collaboration in marine biology as a form of natural history places these discussions in a broader context. When concentrating on growth in marine biology, it becomes clear that the exploration of life in the oceans started hundreds of years ago with relatively small forms of collaboration that developed over time, increasing in scale and scope while also transforming research practice. Contemporary developments in science and society have become integrated in the traditional natural history style of research, transforming the way in which life is measured, mapped and modelled. So although the Human Genome Project might be the first form of big biology in laboratory biology, it has been preceded and accompanied by increasing collaboration in field biology.

This analysis therefore suggests that when talking about big biology, and in order to come to a nuanced understanding of transformations in the organisation of life sciences research, different forms of collaboration in biology have to be taken into account. Such difference can be made through the contrasting of field and laboratory biology, or by looking into different sub-disciplines of biology, e.g. ecology, molecular biology, etc. However, through the notion of different ‘ways of knowing’ Pickstone [3] provides another way to make a distinction between different types of research in biology. While taking natural history as a starting point, he shows how an emphasis on the collection of species in cabinets and museums, gave way to times in which analysis and experimentation became central, together with the emergence of the laboratory as main research site. Distinguishing ways of knowing has the advantage that it connects epistemological and organisational perspectives on research, and can thereby also be used to explicate ‘collective ways of knowing’. These collective ways of knowing attend to various ways of collaborating with different timelines, as becomes visible when comparing for instance collaboration in natural history with more analytical oriented projects in laboratory biology (e.g. the Human Genome Project). Or one could compare different types of natural history collaborations, such as the Census of Marine Life with the Long Term Ecological Research network that monitors and compares life at various sites in the Unites States and Europe.

Next to identifying various forms of collaboration in biology, analysing collective ways of knowing allows for the description of scientific and organisational developments within specific ways of knowing, thereby also showing their interaction and entanglement. For instance, the Census of Marine Life does not only illustrate the development of collaboration in marine biology, but also shows its entanglement with analysis and experimentation in molecular biology through the ways in which more recent developments in laboratory biology transform the identification of species. Moreover, this perspective makes a comparison with collective ways of knowing outside of biology possible, as this typology of collaboration goes beyond the life sciences. For instance, when comparing contemporary large-scale projects in molecular biology and particle physics, a similar focus on the analysis of, and experimentation with, the essential building blocks of respectively life and matter becomes visible. While at the same time a difference in the size of technologies can be noticed, with implications for the organisation of research: while projects in physics centralise around large instruments, projects in molecular biology have a more decentralized character using ICTs to connect the different research sites.

In sum, the analysis of transformations in marine biology speaks to discussions on big biology. It is important to go beyond the polarisation of opponents and proponents of large-scale biology in order to understand the complexity of the transformations in the organisation of the life sciences. Not only the different meanings of big science, but also the different manifestations of collective ways of knowing in biology require attention. When analysing specific ways of knowing life, the complexity of scientific and organisational developments becomes clear, showing how the increase in scale comes in various forms and with different timescales. This more dynamic view on large-scale research, opens the way to a better understanding and a more nuanced outlook on big biology and its diverse manifestations.

Author Contributions

Conceived and designed the experiments: NV. Performed the experiments: NV. Analyzed the data: NV. Wrote the paper: NV.

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The race to discover biodiversity: 11 new marine species and a new platform for rapid species description

Accelerating global change continues to threaten Earth's vast biodiversity, including in the oceans, which remain largely unexplored. To date, only a small fraction of an estimated two million total living marine species have been named and described. A major challenge is the time it takes to scientifically describe and publish a new species, which is a crucial step in studying and protecting these species. The current scientific and publishing landscape often results in decade-long delays (20-40 years) from the discovery of a new species to its official description. As an alternative to this, the Ocean Species Discoveries initiative was launched, offering a new platform for rapid but thorough taxonomic description of marine invertebrate species.

Ocean Species Discoveries is coordinated by the Senckenberg Ocean Species Alliance (SOSA), a project of the Senckenberg Research Institute and Natural History Museum Frankfurt. SOSA's goal is to facilitate the discovery, protection, and awareness of marine invertebrate species before they become extinct.

The project coordinated 25 different researchers and produced data on thirteen marine invertebrate taxa, including one new genus, eleven new species, and one redescription and reinstatement. The species, which originate from all over the globe and at depths from 5.2 to 7081 meters, are brought together in an open-access publication in the Biodiversity Data Journal .

This is the first of a series of publications related to SOSA's initiative, in collaboration with Biodiversity Data Journal, presenting a revolutionary approach in new species descriptions, thanks to which the publication of new species takes years, sometimes even decades, less. The ARPHA publishing platform, which powers the Biodiversity Data Journal, further expedites species descriptions and their use in studies and conservation programs by employing a streamlined data publishing workflow. ARPHA automatically exports all species data, complete with images and descriptions, to GBIF -- the Global Biodiversity Information Facility and the Biodiversity Literature Repository at Zenodo, from where other researchers can easily find and use them.

One of the new species described in the Ocean Species Discoveries is Cunicolomaera grata , a curious amphipod whose burrows along the seafloor perplexed scientists . Another is a wrinkly-shelled limpet called Lepetodrilus marianae that lives on hydrothermal vents, underwater volcanoes in the deep-sea where temperatures can reach 400 degrees C. Normally, the descriptions for these two very different species wouldn't be in the same publication, but this new publication format allows for species descriptions from different marine invertebrate taxa to be published together in one 'mega-publication,' offering a huge incentive for researchers to make their discoveries public.

"Currently, there's a notable delay in naming and describing new animals, often because journals expect additional ecological or phylogenetic insights. This means many marine species go undescribed due to lack of data. OSD addresses this by offering concise, complete taxonomic descriptions without requiring a specific theme, refocusing attention on taxonomy's importance," says Dr. Torben Riehl, who is one of the researchers featured in Ocean Species Discoveries .

Reducing the time it takes to get from discovering a new animal to a public species description is crucial in our era of increasing biodiversity loss. The wrinkly-shelled limpet and two other species described in the Ocean Species Discoveries live in hydrothermal vent zones -- an environment threatened by deep-sea mining. Another OSD species, Psychropotes buglossa, a purple sea cucumber (sometimes also called a gummy squirrel), lives in the North Atlantic, but similar species live in areas of high economic interest, where polymetallic-nodule extraction could soon endanger sea life. Threats like these risk driving species to extinction before we even get the chance to know and study them. Through efforts like SOSA's Ocean Species Discoveries , we can get closer to understanding the biodiversity of our oceans and protecting it before it's too late.

"Only by leveraging the collective strengths of global progress, expertise, and technological advancements, will we be able to describe the estimated 1.8 million unknown species living in our oceans. Every taxonomist specialized on some group of marine invertebrates is invited to contribute to the Ocean Species Discoveries ," says Prof. Dr. Julia Sigwart in conclusion.

• New Species
• Endangered Animals
• Environmental Awareness
• Exotic Species
• Oceanography
• Marine conservation
• Marine biology
• Dinoflagellate
• Permian-Triassic extinction event

Story Source:

Materials provided by Pensoft Publishers . The original text of this story is licensed under a Creative Commons License . Note: Content may be edited for style and length.

Journal Reference :

• Senckenberg Ocean Species Alliance (SOSA), Angelika Brandt, Chong Chen, Laura Engel, Patricia Esquete, Tammy Horton, Anna Jażdżewska, Nele Johannsen, Stefanie Kaiser, Terue Kihara, Henry Knauber, Katharina Kniesz, Jannes Landschoff, Anne-Nina Lörz, Fabrizio Machado, Carlos Martínez-Muñoz, Torben Riehl, Amanda Serpell-Stevens, Julia Sigwart, Anne Helene Tandberg, Ramiro Tato, Miwako Tsuda, Katarzyna Vončina, Hiromi Watanabe, Christian Wenz, Jason Williams. Ocean Species Discoveries 1–12 — A primer for accelerating marine invertebrate taxonomy . Biodiversity Data Journal , 2024; 12 DOI: 10.3897/BDJ.12.e128431

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Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming

Kristy j kroeker.

* Bodega Bay Laboratory, University of California, 2099 Westside Rd, Bodega Bay, CA, 94923, USA

Rebecca L Kordas

† University of British Columbia, Vancouver, BC, Canada, V6T1Z4

‡ Puget Sound Restoration Fund, 590 Madison Ave N, Bainbridge Island, WA, 98110, USA

Iris E Hendriks

§ Global Change department, IMEDEA (CSIC-UIB), Instituto Mediterráneo de Estudios Avanzados, C/Miquel Marqués 21, Esporles (Mallorca), 07190, Spain

Laura Ramajo

¶ Laboratorio de Ecologia y Cambio Climatico, Facultad de Ciencias Universidad Santo Tomas, C/Ejercito, 146, Santiago de Chile

Gerald S Singh

Carlos m duarte.

‖ The UWA Oceans Institute and School of Plant Biology, University of Western Australia, 35 Stirling Highway, Crawley, 6009, Australia

Jean-Pierre Gattuso

** Laboratoire d'Océanographie de Villefranche-sur-Mer, CNRS-INSU, BP 28, Villefranche-sur-Mer Cedex, 06234, France

†† Université Pierre et Marie Curie-Paris 6, Observatoire Océanologique de Villefranche, Villefranche-sur-Mer Cedex, 06230, France

Associated Data

Ocean acidification represents a threat to marine species worldwide, and forecasting the ecological impacts of acidification is a high priority for science, management, and policy. As research on the topic expands at an exponential rate, a comprehensive understanding of the variability in organisms' responses and corresponding levels of certainty is necessary to forecast the ecological effects. Here, we perform the most comprehensive meta-analysis to date by synthesizing the results of 228 studies examining biological responses to ocean acidification. The results reveal decreased survival, calcification, growth, development and abundance in response to acidification when the broad range of marine organisms is pooled together. However, the magnitude of these responses varies among taxonomic groups, suggesting there is some predictable trait-based variation in sensitivity, despite the investigation of approximately 100 new species in recent research. The results also reveal an enhanced sensitivity of mollusk larvae, but suggest that an enhanced sensitivity of early life history stages is not universal across all taxonomic groups. In addition, the variability in species' responses is enhanced when they are exposed to acidification in multi-species assemblages, suggesting that it is important to consider indirect effects and exercise caution when forecasting abundance patterns from single-species laboratory experiments. Furthermore, the results suggest that other factors, such as nutritional status or source population, could cause substantial variation in organisms' responses. Last, the results highlight a trend towards enhanced sensitivity to acidification when taxa are concurrently exposed to elevated seawater temperature.

Introduction

Ocean acidification is projected to impact all areas of the ocean, from the deep sea to coastal estuaries ( Orr et al ., 2005 ; Feely et al ., 2009 , 2010 ), with potentially wide-ranging impacts on marine life ( Doney et al ., 2009 ). There is an intense interest in understanding how the projected changes in carbonate chemistry will affect marine species, communities, and ecosystems ( Logan, 2010 ; Gattuso & Hansson, 2011a ). The rapidly growing body of experimental research on the biological impacts of acidification spans a broad diversity of marine organisms and reveals an even broader range of species' responses, from reduced calcification rates in oysters (e.g., Gazeau et al ., 2007 ; Talmage & Gobler, 2010 ; Waldbusser et al ., 2011 ) to impaired homing ability in reef fishes ( Munday et al ., 2009 , 2010 ) to increased growth rates in macro algae ( Hurd et al ., 2009 ; Koch et al ., 2013 ). Translating the wide range of responses to ecosystem consequences, management actions, and policy decisions requires a synthetic understanding of the sources of variability in species responses to acidification and the corresponding levels of certainty of the impacts.

Meta-analysis is a quantitative technique for summarizing the results of primary research studies. It provides a transparent method to identify key patterns across numerous studies, and can be used to develop hypotheses for future research. Furthermore, it can be a powerful tool for placing individual studies into the context of a broader field of research on a topic. While several meta-analyzes have been published regarding ocean acidification ( Dupont et al ., 2010 ; Hendriks et al ., 2010 ; Kroeker et al ., 2010 ; Liu et al ., 2010 ), research on this topic is growing exponentially ( Gattuso & Hansson, 2011b ). Over 403 studies investigating ocean acidification have been published since the beginning of 2010, which more than triples the number of studies included in any previous meta-analysis of its impacts ( Hendriks et al ., 2010 ; Kroeker et al ., 2010 ; Liu et al ., 2010 ). These new studies provide an important opportunity to expand our understanding of species vulnerability and resilience to ocean acidification by including a broader array of species in the analyzes, as well as an opportunity to test the robustness of the patterns found in previous analyzes and highlight new insights.

Previous meta-analyzes identified significant variation in response to ocean acidification among broad taxonomic groups ( Kroeker et al ., 2010 ) and suggested there is predictable sensitivity among heavily calcified organisms and higher tolerance among more active mobile organisms (e.g., crustaceans and fish). Variation in sensitivity among calcifying taxa was primarily attributed to differences in life history characteristics, including the degree of control over calcification processes ( Berry et al ., 2002 ; Cohen et al . 2009 ), the presence or absence of biogenic coverings that separate calcified material from seawater (e.g., the periostracum in mussels Ries et al ., 2009 ; Rodolfo-Metalpa et al ., 2011 ), or the amount of calcium carbonate in an organism's shell or skeleton ( Kroeker et al ., 2011a ). However, there is still unresolved variation in sensitivity within these taxonomic groups. Determining whether the remaining variation within taxonomic groups is due to species-specific differences that are inherently difficult to predict, or is due to additional methodological or biological factors remains an important area of research.

Several hypotheses regarding the variation in sensitivity to ocean acidification have been proposed that are not directly related to taxonomic characteristics. For example, acidification's effects can differ across life stages of the same species (e.g., Talmage & Gobler, 2010 ; Albright & Langdon, 2011 ; Crim et al ., 2011 ; Martin et al ., 2011 ). Pronounced sensitivity among a particular life history stage could determine the sensitivity of the species as a whole, but previous meta-analyzes were not able to detect clear patterns among life history stages when all taxa were pooled together ( Kroeker et al ., 2010 ). It was proposed that differences among life stages may be apparent within taxonomic groups, but the lack of studies at the early life history stages of many taxa prevented these comparisons ( Kroeker et al ., 2010 ). Therefore, the emergence of numerous studies on larvae in recent years, may allow a re-evaluation of acidification's impacts across different life history stages.

Recent research has highlighted other factors that may underlie variability in sensitivity among and within taxonomic groups. For example, increased food or nutrient supply can offset reductions in calcification and growth associated with acidification in corals ( Cohen et al . 2009 ; Holcomb et al ., 2010 ) and mussels ( Melzner et al ., 2011 ; Thomsen et al ., 2013 ). Furthermore, adaptation can cause one population to be more or less sensitive than another population of the same species ( Langer et al ., 2009 ; Parker et al ., 2011 ). In addition, some species may be able to acclimate to acidification over longer time frames ( Form & Riebesell, 2011 ), suggesting that the duration of the experiment may influence the species response. As research on ocean acidification has progressed, it is important to understand how the variability due to these factors compares to other known sources of variation.

Moreover, the increasing levels of atmospheric CO 2 are concurrently driving ocean warming ( Meehl et al . 2007 ), and a growing number of experiments have tested the combined effect of ocean acidification and warming. Elevated temperatures can increase the metabolic rate of organisms within their thermal tolerance window, but cause a rapid deterioration of cellular processes and performance beyond tolerance limits ( Pörtner, 2008 ). Hence, predicting the combined effects of warming and acidification is difficult, as warming could either offset the effects of ocean acidification ( McCulloch et al ., 2012 ) or aggravate it through an accumulation of stress effects ( Anthony et al ., 2008 ). As a result, meta-analyzes on the impacts of ocean acidification can now extend beyond preceding efforts by addressing the role of warming on the response of marine biota to acidification.

As research has progressed, it is important to examine how new studies influence our understanding of acidification's impacts. Here, we test the robustness of previous conclusions regarding the sensitivity of various taxonomic groups to ocean acidification to an additional 155 studies (representing approximately 100 new species that were not included in the previous meta-analysis ( Kroeker et al ., 2010 ), which had 79 species). In particular, we used meta-analyzes to test: (i) how taxa vary in key physiological responses, as well as changes in abundance to ocean acidification; (ii) how these effects vary across different life stages within common taxonomic groups; and (iii) how increased temperatures influence the effect of acidification across multiple response variables. We then compare these results to previous analyzes and highlight new insights.

Materials and methods

For these analyzes, we repeated the methods reported in Kroeker et al . (2010 ). First, we identified studies that measured any biological response to ocean acidification published from 1 January 2010 to 1 January 2012 by searching ISI web of science and the European Project on Ocean Acidification (EPOCA) blog ( http://oceanacidification.wordpress.com/ ), as well as the literature cited of the identified studies, resulting in 403 published studies.

We included the data from any study that measured a biological response to a 0.5 unit reduction or less in mean seawater pH (on any pH scale), which reduced the 403 studies to 155 studies. The 0.5 unit reduction in pH was chosen to approximate projections for changes in the global mean surface pH in the near future (i.e., 2100) ( Caldeira & Wickett, 2003 ; Caldeira, 2005 ). Although the magnitude of projected pH reductions varies by location and depth ( Feely et al ., 2009 ), we chose the response to a pH change closest to this global projection (<0.5) to minimize experimental variation. However, we then tested the effect of the magnitude of pH changes on our response estimates (see sensitivity analyzes below).

Although multiple carbonate chemistry parameters will change with acidification, we chose to compare responses with mean reductions in pH, because it is the most commonly reported seawater chemistry parameter that allowed us to best standardize comparisons among experiments. In addition, we chose to use a relative change in pH from the control pH designated by the author of each study (rather than particular pH or pCO 2 values) to allow for differences in the ambient (control) conditions in the system of interest. However, there are still many studies that do not adequately characterize the carbonate chemistry for their study system to know if the designated control is ecologically relevant, and instead rely on global mean pCO 2 levels and projections, despite research that has highlighted the wide range of pH values marine organisms are currently experiencing (e.g., Hofmann et al ., 2011 ). While this is an important area for improvement ( McElhany & Busch, 2012 ), we rely on the authors' designations of control pH for the current analysis, which range from pH T 7.8 to 8.2. The pH total scale is used throughout the study when absolute pH values are indicated.

Data from any experiment that factorially manipulated both carbonate chemistry and temperature were also collected. For these experiments, we analyzed responses at ambient and a 2–3 °C elevated temperature treatment to approximate the projected global averages of near-future warming in the surface ocean ( IPCC, 2007 ). While warming is projected to be more extreme in some areas, all studies had similar temperature manipulations (2–3 °C), which allowed us to standardize among studies.

The choice of which studies to include in meta-analysis can profoundly influence the conclusions ( Abrami et al ., 1988 ; Englund et al ., 1999 ; Osenberg et al ., 1999 ). It is recommended that all relevant data are included in the meta-analysis and that decisions regarding whether studies should be included based on judgments of ‘quality’ be minimized due to issues of bias ( Englund et al ., 1999 ). Instead, running and reporting multiple meta-analyzes with various levels of data selection criteria is recommended to test the robustness of the patterns. Thus, all studies that measured a biological response to a 0.5 unit reduction in pH were included, and several analyzes were used to test the role of data selection criteria and potential methodological sources of variation ( Osenberg et al ., 1999 ). Data points and error estimates were obtained from the EPOCA database ( Nisumaa et al ., 2010 ) or interpolated from figures with graphical software ( data thief iii v. 1.5, Amsterdam, the Netherlands; and graphclick v. 3.0, Neuchâtel, Switzerland).

The data set, comprised of 155 studies, which was then merged with another data set (built with the same methods) that was based on studies published prior to 1 January 2010 ( Kroeker et al ., 2010 ). This combined data set had 228 studies, measuring responses of marine organisms to ocean acidification ( Table S1 ). For each study (i.e., a published article), responses from separate experiments (i.e., independent experiments within a published article) at ambient levels of any other factors (e.g., temperature, nutrients, food supply, light levels) were collected. When ambient food concentrations were not reported, we included the responses of the fed/higher nutrient treatments over the unfed/lower nutrient concentrations. In addition, the differences in responses between the fed/high nutrient and unfed/low nutrient responses were compared with the mean effects and variability for given responses.

Responses from separate species in the same experiment (e.g., species allowed to interact in the same tank) were collected separately. Although, the responses of multiple species from the same experiment are not truly independent, we chose to include multiple species responses from a single experiment, because the indirect effects (e.g., species interactions) of acidification that are nonindependent are very pertinent to global acidification scenarios where species will be experiencing both direct and indirect effects. In addition, multiple lines/populations of the same species from the same experiment were all included for similar reasons. Differences between lines/populations of the same species represent real sources of variability that are the focus of this study. The entire data set primarily consisted of experiments on single species, but also included field experiments (e.g., 18 studies from natural gradients and naturally acidified ecosystems and 21 studies using mesocosms with multiple species).

For each experiment, the effect of acidification was calculated as the log-transformed response ratio ( LnRR ). It is the ratio of the mean effect in the acidification treatment to the mean effect in a control group ( Hedges et al ., 1999 ). Then, the overall mean effect was calculated for each response variable (survival, calcification, growth, photosynthesis, development, abundance, and metabolism) by weighing each individual LnRR by the inverse of the sum of its sampling variance and the between experiment variance, and then calculating the weighted mean (i.e., random effects meta-analysis; Hedges & Olkin, 1985 ). Because of the weighting by variance, any experiment that did not report an error estimate was excluded from the random effects meta-analysis. This resulted in 29 responses excluded from the main analyzes (although they were included in a sensitivity analysis; Fig. S1 ). When a single experiment reported several response variables, we included only one response from an experiment per response variable to avoid pseudoreplication. For example, if an experiment reported the effects on calcification, growth rate, and metabolism, each of those responses were included in the separate meta-analyzes for each response. However, if an experiment reported the effects on various metrics of a response type, such as growth rates based on changes in biomass and length, we included only the most inclusive for that response variable (i.e., we chose to use biomass rather than length to represent growth).

Calcification responses were primarily the estimates of net calcification. Growth responses included estimates of change in biomass, length, width, somatic tissue, and growth rates. Photosynthesis responses included changes in the photosynthetic rate or efficiency. Development responses were primarily based on indices of embryonic or larval development (e.g., percent metamorphosed, percent larvae to reach a certain stage, etc.). Abundance responses encompassed the number of individuals, including the number of newly settled individuals, as well as percent cover estimates. Survival rates were typically reported as the final percent survival or mortality at the end of the experiment, which were then converted to survival. In addition to the analyzes on this raw data, the survival data were also converted into specific daily survival rates to account for differences in the duration of the experiments, and unweighted fixed effects meta-analyzes were performed on LnRR estimates on these duration-weighted, daily survival rates ( Fig. S2 ). Because the focus of this study includes only key physiological and ecological parameters, it should be noted that there are likely to be important effects of ocean acidification that are not captured in this analysis. Several studies report the effects of ocean acidification on reproduction (e.g., fertilization success). However, because this is the subject of several qualitative reviews ( Albright, 2011 ; Byrne, 2011 ; Ross et al ., 2011 ), it is not considered here.

Heterogeneity in mean effect sizes was determined by a significant (α = 0.05) Q T statistic, which is calculated by summing the standard deviation of each effect size from the overall mean effect size estimate, and then weighting each one by the inverse of its sampling variance ( Cochran, 1954 ; Rosenberg et al ., 2000 ). Significant heterogeneity ( Q T ) can indicate that there is underlying data structure that is not adequately captured by the mean effect size (e.g., multiple populations of effect sizes rather than just one population of effect sizes), potentially signaling important sources of biological variation.

The variation in effect sizes among (i) taxa; and (ii) life stages within taxonomic groups was tested with categorical random effects meta-analysis ( Hedges & Olkin, 1985 ). For these analyzes, effect sizes were first partitioned into categories (based on taxonomic groups or life stages within taxonomic groups, respectively). Only the response variables with representative studies in the priori defined categories, and only those categories that had four or more data points for the analyzes were included. The statistic Q M (which quantifies the variation explained by the chosen categories vs. the residual variation, which is defined by Q E ) was then computed to determine whether significant variability is explained by the categories ( Hedges & Olkin, 1985 ; Rosenberg et al ., 2000 ). The significance of Q M was tested by a randomization procedure that randomly re-assigns the effect sizes to the categories to create a probability distribution for mean effect sizes of each category using 9999 iterations ( Rosenberg et al ., 2000 ).

Variation in the effects of acidification at ambient and elevated seawater temperatures was tested by analyzing only those studies that factorially compared both factors (i.e., <0.5 unit reduction in pH combined with a 2–3 °C rise in seawater temperature). We only analyzed the effect of acidification at the ambient seawater temperature (identified by the author of the primary study) in the previous analyzes. In the present analysis, a random effects categorical meta-analysis was performed on (i) the effect of acidification at ambient temperature; (ii) the effect of acidification at an elevated temperature for each different response variable. All meta-analyzes were performed with metawin V. 2.0 (Sinauer Associates).

After meta-analyzes, the mean LnRR estimates were back transformed to mean percent change estimates for ease of interpretation. Because each response ratio was natural log-transformed prior to calculating the mean effect size, the antilog of the mean LnRR was taken to calculate a mean response ratio. Back transformations using the antilog provide a geometric mean of the response ratios, which is known to underestimate the arithmetic mean ( Rothery, 1988 ). However, the underestimation of the arithmetic mean is generally very small ( Hedges et al ., 1999 ). Therefore, reported mean percent change transformations can be considered conservative estimates.

Sensitivity analyzes

To examine the robustness of the results, the Rosenthal's fail-safe number was calculated for each analysis. It estimates the number of nonsignificant results needed to change the significance of the meta-analysis. Furthermore, the disproportionate contribution of an individual experiment with a large magnitude effect size to a given result was tested by (i) ranking each experiment by the magnitude of its effect size; and (ii) individually removing each of the five experiments with the largest magnitude effect sizes from the overall analyzes one at a time and re-running the analyzes. If the exclusion of a single experiment changed the significance of the overall mean effect size or the heterogeneity statistic ( Q T ), we would want to consider removing it from the analysis as it would signal a disproportionate contribution to the overall result. However, this was not the case in any analysis, and all experiments were included. Normality was also checked with normal quantile plots, and non-normal distributions were compensated for by testing the significance of Q T and Q M statistics with randomization tests from 9999 iterations of the data and bootstrapped bias-corrected 95% confidence intervals for the mean effect sizes ( Adams et al ., 1997 ).

Unweighted, fixed effects meta-analyzes were also run for each dataset to examine the role of data selection and weighting on the results ( Englund et al ., 1999 ). This allowed the inclusion of studies that did not report error estimates and that were excluded from the weighted analyzes. Finally, differences in effects sizes due to methodological factors, such as length of experiment or magnitude of pH change, were tested with continuous random-effects meta-analysis ( Rosenberg et al ., 2000 ). Separate analyzes were performed for each taxonomic group with more than 10 data points with either duration of experiment or magnitude of pH change as a continuous variable.

When all taxa are pooled together, ocean acidification had a significant negative effect on survival, calcification, growth, development and abundance ( Fig. 1 ; Table S2 ). Overall, survival and calcification are the responses most affected by acidification, with 27% reductions in both responses, whereas growth and development are reduced by approximately 11–19%, respectively, for conditions roughly representing year 2100 scenarios. On average, the abundance is reduced 15%. In contrast, effects of acidification on photosynthesis and metabolism are not detected, when all taxa are pooled together.

Mean effect of near future acidification on major response variables. Significance is determined when the 95% bootstrapped confidence interval does not cross zero. The number of experiments used to calculate the mean is included in parentheses. *denotes a significant effect.

The magnitude of these effects varies among taxa ( Figs 2 – 4 ; Table S3 ). Reductions in survival are similar among corals, mollusks and echinoderms (although only significant for mollusks), whereas no effect is detected for crustaceans. Corals, coccolithophores, and mollusks show the greatest mean reductions in calcification (22–39%), whereas a significant mean effect of acidification is not detected on the calcification of echinoderms or crustaceans. However, these differences among taxonomic groups are not significant sources of variation in this analysis ( Table S3 ). All calcified taxa show similar magnitude mean reductions in growth (9–17% reductions), although these reductions are only statistically significant for mollusks and echinoderms. Effects on fish growth are not detected, whereas growth increases 22% on average among fleshy algae and 18% among diatoms (growth Q M 8,146 = 70.85, P = 0.001). The effects of acidification on photosynthesis vary little among taxa with the exception of calcified algae, for which photosynthesis is reduced 28% on average (photosynthesis Q M 5,61 = 40.88, P = 0.004). This sensitivity in calcified algae is also apparent in experiments that tested for impacts on abundance, where calcified algae have a much greater mean reduction (80%) in percent cover/abundance in acidified conditions than other groups. In addition, corals suffer significant mean reductions in abundance (47%) in acidified treatments, whereas there is very high variability among other taxa (abundance Q M 6,41 = 42.55, P = 0.005).

Variation in effect sizes among key taxonomic groups, divided by major response variables. Note there are different scales on the y-axes to highlight the variation among taxa. Means are from a weighted, random-effects model with bootstrapped bias-corrected 95% confidence intervals. The number of experiments used to calculate the means is given in parentheses. Not all response variables are considered in this analysis. *denotes a significant difference from zero.

Summary of effects of acidification among key taxonomic groups. Effects are represented as either mean percent (+) increase or percent (−) decrease in a given response. Percent change estimates were back transformed from the mean LnRR , and represent geometric means, that are conservative of the arithmetic means.

In addition, acidification reduces the development of the early life stages of mollusks and sea urchins ( Fig. 3 ; bivalves dominate the mollusk category in 9 of 13 experiments). In comparisons among life stages, the mean effect of acidification on mollusk survival was lowest for larvae ( Q M 2,23 = 3.22, P = 0.05; Fig. 5 ; Table S4 ). This pattern is consistent for the effects of acidification on mollusk metabolism (primarily estimated by oxygen consumption); metabolism is significantly reduced among mollusk larvae and unaffected or increased slightly among adults ( Q M 1,13 = 15.82, P = 0.003; Fig. 5 ). No significant differences in effect sizes are detected among life stages within taxonomic groups for any other response (i.e., the Q M statistics are not significant), including survival of echinoderms or crustaceans, calcification of corals or mollusks, or growth of corals, echinoderms or mollusks ( Fig. 5 ; Table S4 ).

Variation in effects of acidification among taxa for development. Means are from weighted, random effects meta-analysis and are shown with bias-corrected bootstrapped 95% confidence intervals. The number of experiments used to calculate each mean is given in parentheses. *denotes a significant difference from zero.

Significant variation in the effects of near-future ocean acidification among lifestages within taxonomic groups. Error bars represent bias-corrected bootstrapped 95% confidence intervals, and the number of experiments used to calculate the means is shown in parentheses. The * associated with mollusk survival and metabolism denotes a significant difference in effect size among life history stages (Significant Q M ).

The duration of the experiments are heavily skewed towards shorter experiments ( Fig. 6 ), making inferences regarding the influence of experiment duration on effect size problematic. For most taxonomic groups, significant effects of experiment duration on effect size are not detected, while in some limited cases, there is a small but significant effect ( Fig. 6 , Table 1 ). However, the limited number of data points at longer durations strongly influences these patterns, and the shape of the distribution of effect sizes are unknown at longer durations.

The effect of experiment duration on log-transformed response ratio from continuous random effect weighted meta-analysis

The effect of duration of experimental CO 2 enrichment on LnRR . The mean effect size and 95% CI (for all taxa pooled) is shown on the left of each figure (overall), while the individual LnRR estimates for each study are plotted against duration (days) on the right side of the figure for survival, calcification, growth, photosynthesis and development.

The influence of the magnitude of the reduction in seawater pH is not consistent across taxonomic groups and response variables. Similar to the duration analyzes, the effect of the magnitude of the pH change is only detected in a limited number of analyzes ( Table 2 ). These effects are very small, differ in the sign of the slope, and are often heavily influenced by a few responses, analogous to statistical outliers ( Figs S3–S6 ).

The effect of the magnitude of pH reduction on log-transformed response ratio from continuous random effects weighted meta-analysis

There is a trend towards lower survival, growth and development (approximately 8–11%) at elevated temperatures, although these differences are not statistically significant ( Fig. 7 ). Elevated temperature has no clear effect on calcification estimates, and there is a nonstatistically significant trend towards higher photosynthesis in response to acidification in the subset of experiments included in this analysis. However, the differences in effect sizes to exposure to acidification at ambient temperature and at elevated temperature do not explain a significant amount of heterogeneity in any dataset ( Table S5 ).

Variation in effect of acidification treatment at ambient temperature and elevated temperature for different response variables . Means are from weighted, random effects categorical meta-analyses for each separate response variable. Error bars represent bias-corrected bootstrapped 95% confidence intervals, and the number of experiments used to calculate the means is shown in parentheses. *denotes a significant difference from zero.

Rosenthal's fail-safe numbers are large for all analyzes, ranging from 192 to 6157, suggesting that the results are robust. Furthermore, there is no change in significance with the singular removal of any of the experiments with large effect sizes. Therefore, all experiments are included in the analyzes. Additionally, all of the unweighted, fixed effects analyzes reveal very similar patterns to their respective weighted, random effects analyzes ( Fig. S1 ). Finally, while the magnitude of effect size in the duration-weighted survival rate is less than the final estimates of survival, both analyzes reveal very similar patterns (e.g., the significance of the mean effect size did not change for any analysis). The effects of acidification on duration-weighted survival rates are reported in Supporting Information ( Fig. S2 ).

Our results reveal reductions in survival, calcification, growth, development, and abundance in response to ocean acidification across a broad range of marine organisms. These results support the findings of previous meta-analyzes ( Kroeker et al ., 2010 ) and suggest that the effect of ocean acidification will be widespread across a diversity of marine life. In addition, the analyzes reveal significant trait-mediated variation in the sensitivity of marine organisms. In general, heavily calcified organisms, including calcified algae, corals, mollusks, and the larval stages of echinoderms, are the most negatively impacted, whereas crustaceans, fish, fleshy algae, seagrasses and diatoms are less affected or even benefit from acidification ( Fig. 4 ) whereas some fleshy algae and diatoms may benefit, although marginally, from the same conditions ( Koch et al ., 2013 ). These results support previous analyzes despite the tripling of studies and the doubling of species included in the analyzes, suggesting that species' traits (taxonomic group) may be a robust factor for forecasting species sensitivity to acidification.

Most of the mean effect size estimates fall within the 95% confidence intervals of the previous meta-analysis ( Kroeker et al ., 2010 ), with the exception of crustaceans. The mean effect of acidification on crustacean calcification and growth fall outside of the previous 95% confidence intervals and are more negative in both cases (although not statistically significant) primarily due to the addition of two studies examining barnacles ( Findlay et al ., 2010a , b ). These results suggest that the growth and calcification of heavily calcified barnacles may be more susceptible to acidification than other mobile crustaceans. Generally, the other mean effect size estimates (those within previous 95% confidence intervals) do not follow directional patterns (i.e., some increase, whereas others decrease slightly) suggesting that reported patterns are robust.

While the broad scale patterns are robust, new insight is gained by examining the body of studies published in recent years. Whereas the mean effect of acidification on mollusks was not significant for any response variable in a previous meta-analysis ( Kroeker et al ., 2010 ), the power provided by the additional 39 recent studies published reveal significant reductions in calcification (40%), growth (17%) and development (25%) of this group. When compared with other taxa, these new results suggest that mollusks are one of the groups most sensitive to acidification ( Fig. 4 ), suggesting the exposure of early life stages of mollusks to acidification may represent a bottleneck for their populations ( Talmage & Gobler, 2010 ; Crim et al ., 2011 ; Hettinger et al ., 2012 ). The slower development of mollusk larvae supports this result as well ( Fig. 3 ). Indeed, the results from the present meta-analysis are consistent with recent evidence suggesting that oyster larvae in hatcheries in the Northeast Pacific Ocean are very sensitive to acidification and are already being impacted by low pH waters ( Barton et al ., 2012 ). Furthermore, recent studies suggest that carry-over effects between life history stages of mollusks can influence the response at later life stages ( Hettinger et al ., 2012 ; Parker et al ., 2012 ).

The increase in the number of studies considering multi-species responses to acidification allows the first synthetic analysis of abundance patterns. Species abundance patterns are of particular interest, because it integrates many of the physiological effects of acidification, as well as indirect effects via species interactions when quantified in a multi-species assemblage. Most of the abundance estimates in this meta-analysis are from multi-species assemblages (75% for mollusks, 90% for corals and 100% for calcifying algae, crustaceans and fleshy algae), with the exception of coccolithophores and diatoms for which the studies are more often focused on specific growth rates of single species. The results reveal considerably more variability in the effects of acidification on abundance than the other response variables (note the large confidence intervals and larger scale in Fig. 2 ), especially among mollusks and crustaceans. This suggests that species interactions may decrease the predictability in species responses ( Fabricius et al ., 2011 ; Hale et al ., 2011 ; Kroeker et al ., 2011b ). Indeed, studies examining impacts of acidification on multi-species assemblages have reported opposing responses of closely related species within the same assemblage, potentially due to compensatory dynamics among the most tolerant species ( Fabricius et al ., 2011 ; Hale et al ., 2011 ; Kroeker et al ., 2011b ; Porzio et al ., 2011 ). Abundance estimates are based upon results from four field studies in three naturally acidified ecosystems, two field mesocosms, and 29 laboratory studies containing multiple species ( Table S1 ), suggesting the results are not biased by a specific approach.

Another important insight in the abundance analysis concerns the early life stages of corals. All abundance estimates for corals used here are focused on the percent settlement of coral spat ( Table S1 ), whereas other response variables mostly estimate the effects of acidification on adult corals. The effect of acidification on coral abundance was greater than its effect on any other response (e.g., abundance is reduced on average 47%, while other response variables are reduced less than 34%). In several studies, this response was dependent on the exposure of the settlement substrate to reduced pH seawater, suggesting ocean acidification affects coral settlement indirectly by affecting the community composition (primarily crustose coralline algae and/or microbial biofilms) or biological and chemical settlement cues ( Albright et al ., 2010 ; Albright & Langdon, 2011 ). These results suggest that the settlement of coral larvae may be particularly sensitive to acidification and could also represent a bottleneck for population dynamics of corals in acidified conditions ( Albright et al ., 2010 ; Albright & Langdon, 2011 ; Doropoulos et al ., 2012 ).

While the effects of acidification on the early life stages of mollusks and coral settlement (abundance) are significant, the sensitivity of early life stages of other taxa are not clear in other categorical meta-analyzes ( Fig. 5 ). These results suggest that the amount of variation due to differences in sensitivity among life stages may be relatively small compared with other sources of variation for some groups. Thus, it is suggested that the identification of potential life history bottlenecks may be best approached at a finer taxonomic resolution for these groups (i.e., quantifying variation in sensitivity of life stages within specific species).

Although the differences between acidification effects at ambient and elevated temperature do not explain a significant amount of variation, there is a trend towards lower survival, growth and development at elevated temperature. Given the significant variation already attributed to taxonomic groups and life history stages, the inability to detect statistically significant differences does not suggest that increased temperature does not affect the response to ocean acidification. It rather suggests that other sources of variation in these analyzes may be more pronounced than the difference in effect size at ambient and elevated temperatures. However, the trend towards lower survival, growth and development on average at elevated temperatures, suggest that continued research on the combined impacts of acidification and warming may be critical for accurately forecasting marine species responses to acidification in the near future.

When all taxa are pooled together, the effects of elevated temperature on species responses to acidification are clearly not apparent for calcification. Modeling efforts have highlighted how warmer temperatures that increase calcium carbonate precipitation kinetics can potentially offset the reduction in calcification caused by lower pH in some species of corals that are able to up-regulate internal pH ( McCulloch et al ., 2012 ). However, this response is limited to certain species and to temperature increases that are within the thermal tolerance of the organism ( Pörtner, 2008 ). Nonetheless, the analysis does contain several studies on corals (10 of 18 experiments examined the response of corals), and increased kinetics due to warmer temperatures could in part explain the insensitivity of the acidification-driven calcification response to increased temperature. Additional studies have suggested that temperature and acidification affect different pathways, with temperature overriding the effects on survival ( Findlay et al ., 2010a ; Lischka et al ., 2011 ) and ocean acidification affecting calcification more specifically. Thus, while there is some evidence for synergistic effects of temperature and acidification in some studies ( Reynaud et al ., 2003 ; Anthony et al ., 2008 ; Rodolfo-Metalpa et al ., 2010 ), our results suggest that this is not the norm in experiments examining their combined impact on calcification (see Comeau et al ., 2010 ).

While the meta-analyzes can explain some variation in responses based on biological traits, the remaining variation within taxonomic groups is still of real ecological interest. Although this remaining variation could represent species-specific sensitivities, the importance of context has recently become more apparent. For example, the responses of both corals and mussels to acidification have been shown to be dependent on their food supply ( Holcomb et al ., 2010 ; Melzner et al ., 2011 ). Although the available studies are few, we found that the difference in LnRR estimates between unfed/low nutrient vs. fed/high nutrient species within in single study can sometimes span or exceed the size of the 95% confidence interval for coral calcification ( Holcomb et al ., 2010 ; Melzner et al ., 2011 ; Edmunds 2011 ). For example, the range of LnRR estimates of coral calcification in zooxanthellate corals ( Astrangia poculata ) between high and low nutrient concentrations (i.e., the difference between high and low nutrient treatments = range = 1.0 LnRR ; Holcomb et al ., 2010 ) is more than double the 95% confidence interval for coral calcification (95% CI = 0.48). However, the range of area-normalized calcification LnRR estimates between Porites spp. with and without heterotrophic feeding (range = 0.22 LnRR ; Edmunds 2012) is about half the 95% CI. In another example, the range of growth estimates of mussels ( Mytilus edulis ) between high and low food concentrations (range = 0.08 LnRR; Melzner et al ., 2011 ) is also approximately half the 95% confidence interval for mollusk growth (95% CI = 0.21 LnRR ). While the examples are few, these results suggests that nutritional status is not trivial in determining species sensitivity to acidification and should be considered to control for sources of variability.

In addition, populations can be locally adapted to different environmental conditions ( Sanford & Kelly, 2010 ) and respond differently to the same acidification stress ( Langer et al ., 2009 ; Sunday et al ., 2011 ; Pistevos et al ., 2011 ; Parker et al ., 2011 ). For example, the range of LnRR estimates for growth among selectively bred lines of the Sydney rock oyster (range = 0.72 LnRR ; Parker et al ., 2011 ) was over three times the 95% confidence interval for the mean effect of acidification on mollusk growth (95% CI = 0.21 LnRR ). In another example, the range of LnRR estimates for growth of different strains of the coccolithophore Emiliania huxleyi (range = 0.47 LnRR ; Langer et al ., 2009 ), almost doubles the 95% confidence interval for coccolithophore growth (95% CI = 0.28 LnRR ). In many cases, the response of a single population is reported as if it was the response of the entire species. As the field progresses, care must be taken into account for and report factors such as location for source populations and background environmental conditions of source populations ( McElhany & Busch, 2012 ) to refine our understanding of acidification's biological impacts.

Despite the growing interest in acclimation to ocean acidification ( Evans & Hofmann, 2012 ), a signal of acclimation is not clear in this data set (i.e., it is not clear whether organisms exposed to acidification for longer durations are less affected than those in short-term experiments). While the analyzes highlight high variability in the short-term experiments, the few experiments at longer durations fall well within the range of effects in short-term experiments and are still well-estimated by the mean effect sizes ( Fig. 6 ). Additional experiments for extended durations, are needed to understand whether the distribution of effect sizes shifts or becomes smaller (i.e., the variability is reduced) over time. However, field studies have shown that species respond to relatively short fluctuations in carbonate chemistry (e.g., diel fluctuations) even when they experience these conditions regularly ( Price et al ., 2012 ). Thus, although short-term studies may not address acclimation potential, the results are still informative and can be ecologically relevant.

While the magnitude of the pH change does not consistently explain a significant amount of variability, it does not necessarily indicate that the magnitude of ocean acidification will not influence species responses. Instead, other sources of variation could be masking a potential relationship between the responses of taxonomic groups and the degree of acidification, including methodological sources of error or true biological sources of variation. In addition, the relationship between the magnitude of pH changes and species responses could be nonlinear, and/or more pronounced changes could be detected in lower pH conditions ( Scheffer & Carpenter, 2003 ; Ries et al ., 2009 ; Christen et al ., 2012 ).

In conclusion, analysis of the rapidly expanding body of research on acidification reveals consistent reductions in calcification, growth, and development of a range of calcified marine organisms, despite the variability in their biology. While our syntheses suggest that some taxa may be predictably more resilient or may benefit from ocean acidification (e.g., brachyuran crustaceans, fish, fleshy algae, and diatoms), it should be noted that a decrease in pH is also likely to have effects that are not captured in the physiological and ecological response variable synthesized here. For example, acidification appears to have neurological effects on fish with repercussions for their behavior ( Nilsson et al ., 2012 ), whereas some marine plants appear to lose the phenolic compounds used as herbivore deterrents under acidified conditions ( Arnold et al ., 2012 ). Furthermore, the potential for acclimation ( Evans & Hofmann, 2012 ) or adaptation ( Sunday et al ., 2011 ; Lohbeck et al ., 2012 ) in response to acidification could potentially lessen the effects on calcified taxa synthesized here and remain critical areas for future research. While physiological effects on these calcified organisms can result in decreases in their abundance, the higher variability in species responses in multi-species studies indicates that species interactions will also be important determinants of abundance ( Fabricius et al ., 2011 ; Kroeker et al ., 2011b ). Furthermore, understanding whether the remaining variation within taxonomic groups and life stages represents real biological differences among species, locally adapted populations, or acclimatory capacities, rather than experimental error, remains a critical area for future research. Finally, marine organisms of the future will not be subjected to acidification in isolation, and our results suggest that continued research on the concurrent effects of warming and acidification is necessary to forecast the status of marine organisms and communities in the near-future.

Acknowledgments

Thanks are due to C.D.G. Harley and two reviewers for comments on an early version of this manuscript and A.-M. Nisumaa for her help with data compilation. This study is a contribution to the European Project on Ocean Acidification (EPOCA) and the MedSeA project (Contract #265103), with funding from the European Community's Seventh Framework Programme. Scientific illustrations are courtesy of the Integration and Application Network ( http://ian.umces.edu/symbols/ ), University of Maryland Center for Environmental Science.

Supporting Information

Additional Supporting Information may be found in the online version of this article:

Figure S1 . Unweighted, fixed effects meta-analyzes.

Figure S2 . Comparison of total percent survival and calculated daily survival rate estimates (weighted by the duration of the study) pooled for all taxa.

Figure S3 . Effect of pH change on LnRR estimates of survival among taxonomic groups.

Figure S4 . Effect of pH change on LnRR estimates of calcification among taxonomic groups.

Figure S5 . Effect of pH change on LnRR estimates of growth among taxonomic groups.

Figure S6 . Effect of pH change on LnRR estimates of photosynthesis among taxonomic groups.

Table S1 . Studies used for analyzes (excel file).

Table S2 . Statistics for overall analyzes.

Table S3 . Statistics for categorical taxonomic analyzes.

Table S4 . Statistics for categorical life stage analyzes within taxonomic groups.

Table S5 . Statistics for categorical temperature analyzes.

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The race to discover biodiversity: 11 new marine species and a new platform for rapid species description

by Pensoft Publishers

A new paper, the Ocean Species Discoveries (OSD), describes a ground-breaking experiment that united 25 independent taxonomists from ten countries. The initiative boasts the discovery of eleven new marine species from all over the globe, occurring at depths from 5.2 to 7081 meters. It also represents a significant step forward in accelerating the pace at which new marine species are described and published.

Accelerating global change continues to threaten Earth's vast biodiversity, including in the oceans, which remain largely unexplored. To date, only a small fraction of an estimated two million total living marine species have been named and described.

A major challenge is the time it takes to scientifically describe and publish a new species, which is a crucial step in studying and protecting these species. The current scientific and publishing landscape often results in decade-long delays (20–40 years) from the discovery of a new species to its official description. As an alternative to this, the Ocean Species Discoveries initiative was launched, offering a new platform for rapid but thorough taxonomic description of marine invertebrate species.

Ocean Species Discoveries is coordinated by the Senckenberg Ocean Species Alliance (SOSA), a project of the Senckenberg Research Institute and Natural History Museum Frankfurt. SOSA's goal is to facilitate the discovery, protection, and awareness of marine invertebrate species before they become extinct.

The project coordinated 25 different researchers and produced data on thirteen marine invertebrate taxa, including one new genus, eleven new species, and one redescription and reinstatement. The species, which originate from all over the globe and at depths from 5.2 to 7081 meters, are brought together in an open-access publication in the Biodiversity Data Journal .

This is the first of a series of publications related to SOSA's initiative, in collaboration with Biodiversity Data Journal, presenting a revolutionary approach in new species descriptions, thanks to which the publication of new species takes years, sometimes even decades, less.

The ARPHA publishing platform, which powers the Biodiversity Data Journal , further expedites species descriptions and their use in studies and conservation programs by employing a streamlined data publishing workflow. ARPHA automatically exports all species data, complete with images and descriptions, to GBIF—the Global Biodiversity Information Facility and the Biodiversity Literature Repository at Zenodo, from where other researchers can easily find and use them.

One of the new species described in the Ocean Species Discoveries is Cunicolomaera grata, a curious amphipod whose burrows along the seafloor perplexed scientists. Another is a wrinkly-shelled limpet called Lepetodrilus marianae that lives on hydrothermal vents , underwater volcanoes in the deep-sea where temperatures can reach 400 degrees C.

Normally, the descriptions for these two very different species wouldn't be in the same publication, but this new publication format allows for species descriptions from different marine invertebrate taxa to be published together in one "mega-publication," offering a huge incentive for researchers to make their discoveries public.

"Currently, there's a notable delay in naming and describing new animals, often because journals expect additional ecological or phylogenetic insights. This means many marine species go undescribed due to lack of data. OSD addresses this by offering concise, complete taxonomic descriptions without requiring a specific theme, refocusing attention on taxonomy's importance," says Dr. Torben Riehl, who is one of the researchers featured in Ocean Species Discoveries.

Reducing the time it takes to get from discovering a new animal to a public species description is crucial in our era of increasing biodiversity loss. The wrinkly-shelled limpet and two other species described in the Ocean Species Discoveries live in hydrothermal vent zones—an environment threatened by deep-sea mining.

Another OSD species, Psychropotes buglossa, a purple sea cucumber (sometimes also called a gummy squirrel), lives in the North Atlantic, but similar species live in areas of high economic interest, where polymetallic-nodule extraction could soon endanger sea life. Threats like these risk driving species to extinction before we even get the chance to know and study them. Through efforts like SOSA's Ocean Species Discoveries, we can get closer to understanding the biodiversity of our oceans and protecting it before it's too late.

"Only by leveraging the collective strengths of global progress, expertise, and technological advancements, will we be able to describe the estimated 1.8 million unknown species living in our oceans. Every taxonomist specialized on some group of marine invertebrates is invited to contribute to the Ocean Species Discoveries," says Prof. Dr. Julia Sigwart in conclusion.

Journal information: Biodiversity Data Journal

Provided by Pensoft Publishers

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Plastic Pollution Affects Sea Life Throughout the Ocean

Photos document extent of the impact, which extends to the seafood people eat.

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Our ocean and the array of species that call it home are succumbing to the poison of plastic. Examples abound, from the gray whale that died after stranding near Seattle in 2010 with more than 20 plastic bags , a golf ball, and other rubbish in its stomach to the harbor seal pup found dead on the Scottish island of Skye, its intestines fouled by a small piece of plastic wrapper.

According to the United Nations, at least 800 species worldwide are affected by marine debris, and as much as 80 percent of that litter is plastic. It is estimated that up to 13 million metric tons of plastic ends up in the ocean each year—the equivalent of a rubbish or garbage truck load’s worth every minute. Fish, seabirds, sea turtles, and marine mammals can become entangled in or ingest plastic debris, causing suffocation, starvation, and drowning. Humans are not immune to this threat: While plastics are estimated to take up to hundreds of years to fully decompose, some of them break down much quicker into tiny particles, which in turn end up in the seafood we eat .

The following photos help illustrate the extent of the ocean plastics problem.

Research indicates that half of sea turtles worldwide have ingested plastic. Some starve after doing so, mistakenly believing they have eaten enough because their stomachs are full. On many beaches, plastic pollution is so pervasive that it’s affecting turtles’ reproduction rates by altering the temperatures of the sand where incubation occurs.

A recent study found that sea turtles that ingest just 14 pieces of plastic have an increased risk of death. The young are especially at risk because they are not as selective as their elders about what they eat and tend to drift with currents, just as plastic does.

Plastic waste kills up to a million seabirds a year. As with sea turtles, when seabirds ingest plastic, it takes up room in their stomachs, sometimes causing starvation. Many seabirds are found dead with their stomachs full of this waste. Scientists estimate that 60 percent of all seabird species have eaten pieces of plastic, a figure they predict will rise to 99 percent by 2050.

While dolphins are highly intelligent and thus unlikely to eat plastic, they are susceptible to contamination through prey that have ingested synthetic compounds.

Plastic in our oceans affects creatures large and small. From seabirds, whales, and dolphins, to tiny seahorses that live in coral reefs… …

... and schools of fish that reside on those same reefs and nearby mangroves.

Plastic waste can encourage the growth of pathogens in the ocean. According to a recent study , scientists concluded that corals that come into contact with plastic have an 89 percent chance of contracting disease, compared with a 4 percent likelihood for corals that do not.

Unless action is taken soon to address this urgent problem, scientists predict that the weight of ocean plastics will exceed the combined weight of all of the fish in the seas by 2050.

Simon Reddy directs The Pew Charitable Trusts’ efforts to prevent ocean plastics.

To Solve the Ocean Plastics Problem, the World Needs a Plan

Beaches littered with soda bottles and single-use takeout containers; rivers choked with plastic bags and cups; microplastics found in the deepest part of the ocean.

Quiz: 9 Startling Facts About Plastics in the Ocean

Up to 13 million tons of plastic waste enters the ocean each year, threatening marine ecosystems and the people who depend on them. Global awareness about plastic pollution has grown tremendously in the last decade as nongovernmental organizations and scientists have better documented the environmental and economic impacts of this material on our marine environment.

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Massive biomolecular shifts occur in our 40s and 60s, Stanford Medicine researchers find

Time marches on predictably, but biological aging is anything but constant, according to a new Stanford Medicine study.

August 14, 2024 - By Rachel Tompa

We undergo two periods of rapid change, averaging around age 44 and age 60, according to a Stanford Medicine study. Ratana21 /Shutterstock.com

If it’s ever felt like everything in your body is breaking down at once, that might not be your imagination. A new Stanford Medicine study shows that many of our molecules and microorganisms dramatically rise or fall in number during our 40s and 60s.

Researchers assessed many thousands of different molecules in people from age 25 to 75, as well as their microbiomes — the bacteria, viruses and fungi that live inside us and on our skin — and found that the abundance of most molecules and microbes do not shift in a gradual, chronological fashion. Rather, we undergo two periods of rapid change during our life span, averaging around age 44 and age 60. A paper describing these findings was published in the journal Nature Aging Aug. 14.

“We’re not just changing gradually over time; there are some really dramatic changes,” said Michael Snyder , PhD, professor of genetics and the study’s senior author. “It turns out the mid-40s is a time of dramatic change, as is the early 60s. And that’s true no matter what class of molecules you look at.”

Xiaotao Shen, PhD, a former Stanford Medicine postdoctoral scholar, was the first author of the study. Shen is now an assistant professor at Nanyang Technological University Singapore.

These big changes likely impact our health — the number of molecules related to cardiovascular disease showed significant changes at both time points, and those related to immune function changed in people in their early 60s.

Abrupt changes in number

Snyder, the Stanford W. Ascherman, MD, FACS Professor in Genetics, and his colleagues were inspired to look at the rate of molecular and microbial shifts by the observation that the risk of developing many age-linked diseases does not rise incrementally along with years. For example, risks for Alzheimer’s disease and cardiovascular disease rise sharply in older age, compared with a gradual increase in risk for those under 60.

The researchers used data from 108 people they’ve been following to better understand the biology of aging. Past insights from this same group of study volunteers include the discovery of four distinct “ ageotypes ,” showing that people’s kidneys, livers, metabolism and immune system age at different rates in different people.

Michael Snyder

The new study analyzed participants who donated blood and other biological samples every few months over the span of several years; the scientists tracked many different kinds of molecules in these samples, including RNA, proteins and metabolites, as well as shifts in the participants’ microbiomes. The researchers tracked age-related changes in more than 135,000 different molecules and microbes, for a total of nearly 250 billion distinct data points.

They found that thousands of molecules and microbes undergo shifts in their abundance, either increasing or decreasing — around 81% of all the molecules they studied showed non-linear fluctuations in number, meaning that they changed more at certain ages than other times. When they looked for clusters of molecules with the largest changes in amount, they found these transformations occurred the most in two time periods: when people were in their mid-40s, and when they were in their early 60s.

Although much research has focused on how different molecules increase or decrease as we age and how biological age may differ from chronological age, very few have looked at the rate of biological aging. That so many dramatic changes happen in the early 60s is perhaps not surprising, Snyder said, as many age-related disease risks and other age-related phenomena are known to increase at that point in life.

The large cluster of changes in the mid-40s was somewhat surprising to the scientists. At first, they assumed that menopause or perimenopause was driving large changes in the women in their study, skewing the whole group. But when they broke out the study group by sex, they found the shift was happening in men in their mid-40s, too.

“This suggests that while menopause or perimenopause may contribute to the changes observed in women in their mid-40s, there are likely other, more significant factors influencing these changes in both men and women. Identifying and studying these factors should be a priority for future research,” Shen said.

Changes may influence health and disease risk

In people in their 40s, significant changes were seen in the number of molecules related to alcohol, caffeine and lipid metabolism; cardiovascular disease; and skin and muscle. In those in their 60s, changes were related to carbohydrate and caffeine metabolism, immune regulation, kidney function, cardiovascular disease, and skin and muscle.

It’s possible some of these changes could be tied to lifestyle or behavioral factors that cluster at these age groups, rather than being driven by biological factors, Snyder said. For example, dysfunction in alcohol metabolism could result from an uptick in alcohol consumption in people’s mid-40s, often a stressful period of life.

The team plans to explore the drivers of these clusters of change. But whatever their causes, the existence of these clusters points to the need for people to pay attention to their health, especially in their 40s and 60s, the researchers said. That could look like increasing exercise to protect your heart and maintain muscle mass at both ages or decreasing alcohol consumption in your 40s as your ability to metabolize alcohol slows.

“I’m a big believer that we should try to adjust our lifestyles while we’re still healthy,” Snyder said.

The study was funded by the National Institutes of Health (grants U54DK102556, R01 DK110186-03, R01HG008164, NIH S10OD020141, UL1 TR001085 and P30DK116074) and the Stanford Data Science Initiative.

• Rachel Tompa Rachel Tompa is a freelance science writer.

About Stanford Medicine

Stanford Medicine is an integrated academic health system comprising the Stanford School of Medicine and adult and pediatric health care delivery systems. Together, they harness the full potential of biomedicine through collaborative research, education and clinical care for patients. For more information, please visit med.stanford.edu .

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• Published: 17 March 2021

Protecting the global ocean for biodiversity, food and climate

• Enric Sala   ORCID: orcid.org/0000-0003-4730-3570 1 ,
• Juan Mayorga   ORCID: orcid.org/0000-0003-1961-8313 1 , 2 ,
• Darcy Bradley   ORCID: orcid.org/0000-0003-2581-8768 2 ,
• Reniel B. Cabral   ORCID: orcid.org/0000-0002-1137-381X 2 ,
• Trisha B. Atwood   ORCID: orcid.org/0000-0001-7153-5190 3 ,
• Arnaud Auber   ORCID: orcid.org/0000-0002-8415-1652 4 ,
• William Cheung   ORCID: orcid.org/0000-0001-9998-0384 5 ,
• Christopher Costello   ORCID: orcid.org/0000-0002-9646-7806 2 ,
• Francesco Ferretti 6 ,
• Alan M. Friedlander 1 , 7 ,
• Steven D. Gaines   ORCID: orcid.org/0000-0002-7604-3483 2 ,
• Cristina Garilao 18 ,
• Whitney Goodell 1 , 7 ,
• Benjamin S. Halpern   ORCID: orcid.org/0000-0001-8844-2302 9 ,
• Audra Hinson   ORCID: orcid.org/0000-0002-4231-4820 3 ,
• Kristin Kaschner 8 ,
• Kathleen Kesner-Reyes 10 ,
• Fabien Leprieur 11 ,
• Jennifer McGowan   ORCID: orcid.org/0000-0001-9061-3465 12 ,
• Lance E. Morgan 13 ,
• David Mouillot   ORCID: orcid.org/0000-0003-0402-2605 11 ,
• Juliano Palacios-Abrantes   ORCID: orcid.org/0000-0001-8969-5416 5 ,
• Hugh P. Possingham   ORCID: orcid.org/0000-0001-7755-996X 14 ,
• Kristin D. Rechberger 15 ,
• Boris Worm 16 &
• Jane Lubchenco   ORCID: orcid.org/0000-0003-3540-5879 17  

Nature volume  592 ,  pages 397–402 ( 2021 ) Cite this article

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Matters Arising to this article was published on 20 September 2023

Matters Arising to this article was published on 10 May 2023

Matters Arising to this article was published on 06 July 2022

An Author Correction to this article was published on 08 April 2021

This article has been updated

The ocean contains unique biodiversity, provides valuable food resources and is a major sink for anthropogenic carbon. Marine protected areas (MPAs) are an effective tool for restoring ocean biodiversity and ecosystem services 1 , 2 , but at present only 2.7% of the ocean is highly protected 3 . This low level of ocean protection is due largely to conflicts with fisheries and other extractive uses. To address this issue, here we developed a conservation planning framework to prioritize highly protected MPAs in places that would result in multiple benefits today and in the future. We find that a substantial increase in ocean protection could have triple benefits, by protecting biodiversity, boosting the yield of fisheries and securing marine carbon stocks that are at risk from human activities. Our results show that most coastal nations contain priority areas that can contribute substantially to achieving these three objectives of biodiversity protection, food provision and carbon storage. A globally coordinated effort could be nearly twice as efficient as uncoordinated, national-level conservation planning. Our flexible prioritization framework could help to inform both national marine spatial plans 4 and global targets for marine conservation, food security and climate action.

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Balancing protection and production in ocean conservation

Integrated ocean management for a sustainable ocean economy

Rebuilding marine life

Data availability.

The underlying data used in this study are available from the sources listed in the  Supplementary Information .

Code availability

The R code that supports the findings of this study is available at https://github.com/emlab-ucsb/ocean-conservation-priorities .

Change history

08 april 2021.

A Correction to this paper has been published: https://doi.org/10.1038/s41586-021-03496-1

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Acknowledgements

This study was funded by the National Geographic Society and the Leonardo DiCaprio Foundation. D.M. was supported by the French Foundation for Research on Biodiversity (FRB).

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Pristine Seas, National Geographic Society, Washington, DC, USA

Enric Sala, Juan Mayorga, Alan M. Friedlander & Whitney Goodell

Environmental Market Solutions Lab, University of California Santa Barbara, Santa Barbara, CA, USA

Juan Mayorga, Darcy Bradley, Reniel B. Cabral, Christopher Costello & Steven D. Gaines

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Trisha B. Atwood & Audra Hinson

IFREMER, Unité Halieutique de Manche et Mer du Nord, Boulogne-sur-Mer, France

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Changing Ocean Research Unit, Institute for the Oceans and Fisheries, The University of British Columbia, Vancouver, British Columbia, Canada

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Hawai‘i Institute of Marine Biology, Kāne‘ohe, HI, USA

Alan M. Friedlander & Whitney Goodell

Evolutionary Biology and Ecology Laboratory, Albert Ludwigs University, Freiburg, Germany

Kristin Kaschner

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E.S., J. Mayorga, D.B., R.B.C., T.B.A., W.C., C.C., F.F., A.M.F., S.D.G., W.G., B.S.H., J. McGowan, D.M., H.P.P., K.D.R., B.W. and J.L. conceived the study and designed the prioritization framework; J. Mayorga, R.B.C., T.B.A., A.A., W.C., A.M.F., C.G., W.G., B.S.H., A.H., K.K., K.K.-R., F.L., L.E.M., D.M., J.P.-A. and B.W. provided data and/or conducted analyses; J. Mayorga, D.B., R.B.C. and A.H. wrote computer code; and E.S., J. Mayorga, D.B., R.B.C., T.B.A., W.C., C.C., F.F., A.M.F., S.D.G., W.G., B.S.H., J. McGowan, L.E.M., D.M., H.P.P., K.D.R., B.W. and J.L. wrote the paper.

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Sala, E., Mayorga, J., Bradley, D. et al. Protecting the global ocean for biodiversity, food and climate. Nature 592 , 397–402 (2021). https://doi.org/10.1038/s41586-021-03371-z

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Received : 19 December 2019

Accepted : 18 February 2021

Published : 17 March 2021

Issue Date : 15 April 2021

DOI : https://doi.org/10.1038/s41586-021-03371-z

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