INTRODUCTION
1. The fair-trade approach presents itself as an alternative strategy, positioned between free trade
and protectionism, to address the issue of poverty in developing countries. It also offers an alternative
way for consumers to express their opinion through “political consumerism” or “responsible
consumerism”. People buying fair-trade products are portrayed as using their consumer choice to
voice their concerns about poverty in less developed countries, and about a trading system that is
considered as unfavourable to these countries. Focusing on the food commodity market is a natural
choice for the fair-trade movement because most developing countries are dependent on these products
for export earnings.

2. In 1988, the first fair-trade labelled product (coffee) was launched under the Max Havelaar
brand. Since then, fair-trade has been growing at a rapid pace and now covers various products, such
as cocoa and chocolate, coffee, bananas, tea, honey products, textiles and handicrafts. Cocoa sold with
the fair-trade label captures a very small share of the cocoa market (0.1 percent). However, based on
the steady growth of fair-trade and the support of public opinion and governments, some fair-trade
participants claim that the idea will move beyond niche markets and become more mainstream.

3. Under Action 9 of its work programme of September 2004, the Consultative Board on the World
Economy requested the ICCO secretariat to undertake an analysis of the situation and prospects for
fair-trade cocoa and its potential market effects. The objective of the Board, according to the work
programme of the Board (document CB/3/2 Rev.1), is to assess whether “a very significant increase in
the tonnages of cocoa beans sold under the fair-trade brand, and therefore at the fair-trade premium
price, would lead to cocoa oversupply and/or depressed demand for non-fair-trade cocoa”.

4. This first document on fair-trade prepared by the ICCO secretariat provides only the basic facts
on fair-trade in cocoa; the volumes traded, the characteristics of the “fair-trade price” and the
additional benefits and costs of this approach. It is envisaged that the factual information on fair-trade
in cocoa provides a good basis for the Board to give guidance to future work by the secretariat.

THE KEY PARTICIPANTS IN THE FAIR-TRADE MOVEMENT AND DEFINITION

5. The fair-trade movement began to take its current form in the 1960s. It is united in the view that
conventional trading relations between the South and the North are unfair and unsustainable and that
this issue can be addressed through a different approach to the trading system. Its goal is to tackle
poverty in developing countries through trade and its pragmatic approach is one of the key reasons for
its success. However, the diversity of the movement, its lack of structure and economies of production
scale was an impediment to its sustainability. Since the early 1990s, the fair-trade movement has
become more organized to address the challenges it faces. The harmonization of definitions, the
increased professionalism and emphasis on quality assurance, the direct marketing through
supermarkets and the establishment of working relations with mainstream businesses to enable
economies of scale, have further secured steady growth of fair-trade.

6. The organizations engaged in fair-trade can be divided into three groups:
• The network and umbrella organizations of the fair-trade movement, which consist of the
following four organizations: the Fairtrade Labelling Organization (FLO), the International
Fair-trade Association (IFAT), the European Fair-trade Association (EFTA) and the Network
of European Worldshops (NEWS). The Fairtrade Labelling Organization (FLO) was
established in 1997, and is the worldwide fair-trade standard setting and certification
organization. Since 2004, it has been composed of two independent bodies, FLO-I for
standard setting and FLO-Cert Ltd. for fair-trade certification and auditing activities. The
FLO has established common principles, procedures and specific certification requirements
for fair-trade and certifies mainly commodity products.

This relates partially to the fact that non-commodity products are usually not subject to direct comparison of price and quality. The FLO deals with cocoa, as well as with coffee, bananas, tea, honey products, rice, fresh
fruits, juices, sugar, sport balls, wine and flowers. It estimates its total retail sale value at
$500 million in 2004. The FLO membership consists of the 19 National Initiatives located
across Europe, North America, Mexico and Australia/New Zealand, as listed in Table 1 and
has recently introduced a common label to be applied across all products in all countries.
The International Fair-trade Association (IFAT) was established in 1989 and is a worldwide
membership organization that brings together both producers and buyers. It is a federation to
promote fair-trade and a forum for exchanging information to help members increase benefits
for producers. It consists of approximately 110 producer organizations and 50 buying
organizations. The Network of European Worldshops (NEWS!), established in 1994, acts as
the umbrella body for the approximately 2,700 “world shops” that sell predominantly

fairtrade goods across Europe. The European Fair-trade Association (EFTA), established in
1990, is an association of 12 importing organizations in nine European countries across
Europe.

• The Southern producer organisations, which supply the products, are traditionally cooperatives or associations. Presently, 15 have the FLO certification to sell cocoa beans under the fair-trade label. While cocoa is mainly produced in Africa (71%), 12 FLO registered cocoa producer associations are located in the Latin American and Caribbean region. FLO registered traders only buy part of the cocoa beans produced by the participating cooperatives. The remainder is sold in the mainstream market. Table 2 provides an exhaustive list of the producer organizations with their main characteristics.

• The fair-trade importing organizations, known as Alternative Trading Organisations (ATOs)
are traditionally non-governmental organizations (NGOs) in Northern countries. These are
the buying organizations, which act as importers, wholesalers and retailers of the products
purchased from the producer organizations. They focus on improving market access and
strengthening producer organizations. In Europe, they sell their products through “world
shops”, local groups, campaigns, wholesale and mail-order catalogues. Table 3 provides an
exhaustive list of the 47 FLO registered cocoa traders.

7. There have been various definitions of fair-trade developed in the past. However, in an attempt
to produce a widely accepted definition, an informal group of umbrella bodies and network organizations called FINE (composed of FLO, IFAT, EFTA and NEWS) has defined fair-trade as follows: “Fair-trade is a trading partnership based on dialogue, transparency and respect, that seeks greater equity in international trade. It contributes to sustainable development by offering better trading conditions to, and securing the rights of, marginalized producers and workers – especially in the South. Fair-trade organizations (backed by consumers) are engaged actively in supporting
producers, awareness raising and in campaigning for changes in the rules and practice of
conventional international trade.” 

THE COMPONENTS OF FAIR-TRADE
8. The FLO approved producer organizations must comply with a number of requirements. Only
organizations of small farmers can be given the FLO certification. The FLO fair-trade standards for
cocoa require the following :
• The fair-trade activity is to promote the “social development” of the organizations. To this
end, the FLO certified producer organizations have to consist mainly of farmers managing
their own farms and the organizations must have a democratic and transparent structure.
• The fair-trade activity is supposed to enhance the “economic development” of the
organization. To this end, the FLO certified producer organizations must have the capacity to
export their production to strengthen their business operations. Moreover, the fair-trade
premium is supposed to be managed democratically.
• Under the heading of “environmental development”, the FLO registered producer
organizations have to include the environment in farm management. More specifically, the
use of certain listed pesticides is prohibited and the production of organic cocoa beans is
encouraged.
• Working conditions in FLO registered producer associations have to follow the International
Labour Organisation (ILO) Conventions. The FLO “standard on labour conditions”
describes how child labour can be used, as well as the requirements in terms of freedom of
association and collective bargaining. All farm workers have to work in a safe environment
and under fair conditions of employment, especially regarding wages.

BENEFITS AND COSTS ASSOCIATED WITH FAIR-TRADE AT THE PRODUCER LEVEL
9. The most essential characteristic of fair-trade is that producer organizations receive a higher
price for their cocoa beans. The fair-trade price represents the necessary condition for the producer
organizations to have the financial ability to fulfil the above requirements, and to cover the
certification fees. The differential in the price of cocoa beans between the conventional market and the
fair-trade market represents the consumers’ willingness to pay for a certified product. The fair-trade
prices are calculated on the basis of world market prices, plus fair-trade premiums. The fair-trade
premium for standard quality cocoa is US$150 per tonne. The minimum price for fair-trade standard
quality cocoa, including the premium, is US$1,750 per tonne. If the world market price of the
standard qualities rises above US$1600 per tonne, the fair-trade price will be the world market price
plus US$150 per tonne.

FLO cocoa price per tonne =
Max {FLO floor price (US$1600); f.o.b. market price} + premium (US$150)
Chart 1 provides the f.o.b. prices for fair-trade cocoa beans that purchasers had to pay during the
September 1998 – February 2005 period and the corresponding monthly averages of the ICCO daily
prices, which reflect the prices of cocoa beans in the London and New York futures markets. It is
obvious that the incentive to sell under the fair-trade market for producers and, conversely, the
opportunity cost for fair-trade purchasers is higher during periods of low market prices, as was the case
in 1999-2001.

10. The “fair-trade price” or “FLO price” represents the price received by the co-operatives. The use
of the funds derived from the premium (US$150 per tonne) is decided by the General Assembly of the
Co-operatives, which is required to act with total transparency. A proportion of the premium may be
paid out to farmers but, in general, it is pooled in a social fund for the benefit of the community rather
than passed on directly to the farmers. The money is used for either cocoa related projects, such as
farmer training and creation of nurseries for new planting materials, or for social projects, such as
boreholes, schools and other investments. These benefit the whole community or the farmers
specifically.

11. In contrast to the premium of US$ 150 per tonne, there are no prescriptions under the fair-trade
arrangements on the use of the difference between the FLO minimum price of US$ 1,750 per tonne
minus premium (US$ 150) and the mainstream price. For example, if the mainstream market price is
US$ 1,200 per tonne, the difference with the FLO minimum price minus premium is US$ 400 per
tonne. It is up to the individual co-operative to decide on the use of these funds.

12. It is further noted that, in most cases, the farmers, at the moment of selling to their co-operatives,
receive the same price for their cocoa as when the co-operative sells mainstream cocoa. In most cases,
the co-operatives pay the same price to all farmers and they sell only part of their total trade volume
under the fair-trade arrangement. The co-operatives do not know which farmers have delivered to
them the cocoa they sell under their fair-trade arrangements. The situation naturally leaves open the
possibility for a co-operative to distribute advantages of the fair-trade arrangements among all their
members.
13. The cost of compliance includes the fees paid by the farmer organizations to the fair-trade
organization and indirect costs to comply with the FLO requirements. The cost of certification used to
be borne by the importers and not the producers. This made the FLO certification unique, by passing
the whole cost of the certification to the buyer. However, since December 2004, both registered
producer associations and traders have to support certification fees, mainly to provide additional
resources to the newly created FLO-Cert Ltd. For traders, as stated in Table 4, the costs are composed
of an initial application fee (up to €2 000 and payable only once) and an annual certification fee (up to
€3 000) dependent upon the total turnover of the trading company.

To get the FLO certification, producer organizations have first to pay an initial application fee (up to €5 200 and payable only once). For the following years, the fee is composed of a fixed amount (€500 per year), and a variable amount
depending on the value of cocoa sold under fair-trade (0.45% of the f.o.b. value), as shown in Table 5.
This implies that a co-operative, which sells 50 tonnes of cocoa in one season has to pay fees of
US$ 20 per tonne. With a fair-trade turnover of 500 tonnes the average fee is cut in half, amounting to
US$ 10 per tonne.

14. Financial benefits and additional costs for co-operatives associated with fair-trade, compared to
the conventional market are summarized below:

Sources of additional benefits
• Fair-trade price: the f.o.b. price paid to the co-operative is higher than the
conventional price and, by definition, more stable.
• Direct sales: the fair-trade supply chain does not usually involve as many
intermediaries as the conventional one.

Source of additional costs
• Cost of participation in the FLO system: certification fees, documentation costs, etc.
• Production costs to meet the FLO standards: possible additional labour, social and
environmental costs.

The size of the fair-trade market
15. FLO registered cocoa producer associations and National Initiatives have to report to FLO,
respectively, on their sales of cocoa beans and cocoa semi-finished products and sales of chocolate and
chocolate products under the fair-trade label. The corresponding volumes are modest, representing
less than 0.1% of the total cocoa market. In 2003, producers sold 2 687 tonnes of cocoa beans and
cocoa semi-finished products, in beans equivalent, under the fair-trade label. Table 6 gives an
overview of the share of total exports of fair-trade cocoa by country of origin during the period 1994-
2003.

As country information on sales is related to a very limited number of co-operatives in some
cases, the disclosure of volumes would have been against the FLO confidentiality policy. In 2003,
more than 90% of the sales originated from two producers: Kuapa Kokoo Ltd. (Ghana) and Conacado
Inc. (Dominican Republic). Consequently, the nine other producers concerned in 2003 sold less than
10% of the total, representing less than 200 tonnes. This highly concentrated market may be the result
of lower costs associated with trading for larger cocoa producers. Since 2003, five new small cooperatives in Peru, and a large one in Côte d’Ivoire have received the fair-trade certification. In Peru,
this is mainly the result of an ongoing United Nations programme to convert coca producers to
alternative crops.

16. Until 2003, cocoa and chocolate products were sold in the fair-trade market in 16 countries,
mainly in Europe. Table 7 provides sales information by country during the 1994-2003 period.
Presently, only information on total sales of chocolate and chocolate products is available, as the
National Initiatives do not provide detailed data on the cocoa content of these products. In 2003, 80%
of the total sales of chocolate and chocolate products were realized in only five countries, the
United Kingdom (35%), Italy (13%), Germany (13%), Switzerland (10%) and France (nine per cent).
Since 2004, fair-trade chocolate and chocolate products have also been sold in Japan, Australia,
New Zealand and Mexico. As shown in Table 8, the estimated market share of fair-trade labelled
cocoa in each country of destination is less than one per cent, with the highest shares (0.9%) in
Switzerland and Luxembourg.

17. Fair-trade certified chocolate and chocolate products are composed of various ingredients. It is
not always possible for all these ingredients to be sourced from a fair-trade-certified producer
organization and consequently for a chocolate product to be “fully fair-trade”. FLO policy defines the
conditions that allow a composite product to carry the fair-trade label. It is stated that all the
ingredients for which the certification exists must be sourced from fair-trade certified producer
organizations and 50% of all the ingredients, by dry weight, must be sourced from fair-trade, certified
producer organizations. However, exceptions to this rule exist as many manufacturers find it difficult
to strictly apply this rule. The implementation of these exemptions requires FLO approval.

Islands are at the forefront of the extinction crisis, with invasive vertebrates as the primary driver of extinctions and threatening nearly half of our world’s most endangered species [7]. Extensive research has recognized the negative impacts that invasive species have on islands with emerging research documenting effects on the surrounding marine ecosystems through predation of native species and degradation of critical ecosystem functions. It has been well established that invasive species can negatively impact local economies, food security, and health through crop damage and erosion, and as vectors for zoonotic disease transmission. These effects are especially relevant for islands with developing economies and limited economic development opportunities.

Invasive rats present on Floreana Island, Galapagos contribute to food insecurity through damage of subsistence crops. Credit: Andrew Wright

We’ve long understood that there are benefits to removing invasive species from island ecosystems for both the conservation of native wildlife and for the people who live in these communities.” stated co-author Dr. Nick Holmes of The Nature Conservancy, “By aligning this conservation tool with the United Nations goals for sustainable development, we are able to draw clear lines between human health and economic benefit to give communities more data for decision-making.”

The removal of invasive species is one of the most effective conservation initiatives available, with more than 1,200 invasive mammal eradications attempted on islands worldwide and an average success rate of 85% [2]. As a proven conservation tool, eradication has repeatedly been shown to revive island ecosystems and pull wildlife back from the brink of extinction. As practitioners pursue restoration on more complex, inhabited islands, it is critical to understand the implications for island communities and sustainable development goals.

Research indicates that seabird islands without invasive rats contribute to healthier coral reef ecosystems with greater resilience to climate change and increased fish biomass. Credit: Island Conservation

This study sought to identify how invasive vertebrate eradications could aligned with the United Nations framework for sustainable development which outlines 17 goals with 169 specific targets, including improving human health, biodiversity conservation, and socioeconomic benefits. By analyzing historical successes, the researchers found that the eradication of invasive vertebrates from islands contributes to 13 SDGs and aligns with up to 25% of the global targets. The team analyzed 292 islands where future eradications are a priority for biodiversity conservation and are considered possible within the next decade or would be possible with advances in technology [4]. In comparing past and future projects, researchers found that moving forward projects are likely to align with more sustainable development targets than they have in the past, which is attributed to the fact that, until recently, practitioners have predominantly restored uninhabited islands. Additionally, the team noted that restoration of islands that are used by nearby communities but not inhabited also present opportunities for sustainable development that encompass island communities beyond those studied.

Community involvement within island restoration projects not only ensures that the voices of communities contribute to decision making, but also provide job and skill training, increasing capacity for these kinds of projects within the region. Credit: Island Conservation

A Global Priority for People and the Planet

These findings suggest an opportunity for investment in the removal of invasive vertebrates from islands as a method for improving human well-being through health and economic development in addition to curbing the extinction crisis and fighting climate change. Invasive vertebrate eradication on islands is an effective conservation tool and often one-time intervention that can build more resilient and sustainable ecosystems and human communities. Unlike many conservation and social interventions, results from invasive species eradication often occur over relatively short time frames; the rapid-results and numerous benefits are particularly significant for islands and communities with developing economies and those facing growing environmental uncertainty.

Eradication of invasive species is a critical tool for stemming the extinction crisis and has been touted as a ‘conservation silver bullet,’ capable of incredible environmental gains for island wildlife and native ecosystems, but beyond preventing extinctions, it is increasingly important to understand the implications for people and island communities,” said Dr. Karen Poiani, Island Conservation CEO.

By identifying the applications for eradication to promote human well-being and biodiversity conservation, the researchers hope to encourage investment and innovation in the field. As eradication efforts increase in scope and scale, it is essential that biodiversity conservation supports the sustainable development of islands, contributing to improved human health and well-being, economic development, education, and the future of life on Earth.

Additional Background

• Invasive species devour eggs, young and even adults of native animals and plants, spread invasive seeds, and destroy vegetation [3,8,6].
• Islands offer hope that we can prevent extinctions and protect biodiversity.
• Eradication of invasive mammals from islands is a proven conservation tool [9].
• Larger, more remote and technically challenging islands are being successfully cleared of invasive species populations each year.
• Many of these investments have resulted in remarkable stories of restoration success, including the recovery of globally threatened species [5].
• Protecting island wildlife and improving the resiliency and sustainability of natural and cultural resources for island communities will require innovative new tools to increase the scale, scope, and pace of restoration to match the magnitude of this conservation challenge [1].

About the partners

Island Conservation is the only global, not-for-profit conservation organization whose mission is to prevent extinctions by removing invasive species from islands. We work where the concentration of both biodiversity and species extinction is the greatest – islands. Removing a primary threat – introduced invasive vertebrates – is one of the most critical interventions for saving threatened plants and animals and restoring island ecosystems. Once invasive species are removed, native island species and ecosystems can recover, often with little additional intervention. To date, we have successfully restored 64 islands worldwide, benefiting 1195 populations of 487 species and subspecies. Island Conservation is headquartered in Santa Cruz, CA, with field offices in British Columbia, Chile, Ecuador, Hawai’i, New Zealand, Palau, and Puerto Rico.

Pacific Rim Conservation’s mission is to maintain and restore native bird diversity, populations, and habitats in Hawaii and across the Pacific region. Founded in 2006, we work together with local communities, government agencies, and other conservation organizations to achieve these goals through predator control and avian translocation techniques. Throughout all of our work, we strive to use a science-based approach to management, using research to improve our methods and inform future conservation actions. To date, we have published more than 120 peer-reviewed papers in high-profile scientific journals and have had our work featured in media outlets such as the New York Times, National Geographic and the BBC.

The Nature Conservancy is a global conservation organization dedicated to conserving the lands and waters on which all life depends. Guided by science, we create innovative, on-the-ground solutions to our world’s toughest challenges so that nature and people can thrive together. We are tackling climate change, conserving lands, waters and oceans at an unprecedented scale, providing food and water sustainably and helping make cities more sustainable. Working in 72 countries, we use a collaborative approach that engages local communities, governments, the private sector, and other partners. To learn more, visit  www.nature.org or follow @nature_press on Twitter.

Resources

1. Campbell, K. J., J. Beek, C. T. Eason, A. S. Glen, J. Godwin, F. Gould, N. D. Holmes, G. R. Howald, F. M. Madden, J. B. Ponder, D. W. Threadgill, A. S. Wegmann, and G. S. Baxter. 2015. The next generation of rodent eradications: Innovative technologies and tools to improve species specificity and increase their feasibility on islands. Biological Conservation 185:47-58.
2. DIISE. The Database of Island Invasive Species Eradications, developed by Island Conservation, Coastal Conservation Action Laboratory UCSC, IUCN SSC Invasive Species Specialist Group, University of Auckland and Landcare Research New Zealand. http://diise.islandconservation.org 2014.
3. Doherty TS, Glen AS, Nimmo DG, Ritchie EG, Dickman CR. Invasive predators and global biodiversity loss. Proceedings of the National Academy of Sciences. 2016;113(40):11261-5.
4. Holmes ND, Spatz DR, Oppel S, Tershy B, Croll DA, et al. (2019) Globally important islands where eradicating invasive mammals will benefit highly threatened vertebrates. PLOS ONE 14(3): e0212128. https://doi.org/10.1371/journal.pone.0212128
5. Jones HP, Holmes ND, Butchart SHM, Tershy BR, Kappes PJ, Corkery I, et al. Invasive mammal eradication on islands results in substantial conservation gains. Proceedings of the National Academy of Sciences. 2016;113:4033–8.
6. Medina FM, Bonnaud E, Vidal E, Tershy BR, Zavaleta ES, Donlan CJ, et al. A global review of the impacts of invasive cats on island endangered vertebrates. Global Change Biology. 2011;17(11):3503-10.
7. Spatz, D. R., Zilliacus, K. M., Holmes, N. D., Butchart, S. H., Genovesi, P., Ceballos, G., … & Croll, D. A. (2017). Globally threatened vertebrates on islands with invasive species. Science Advances, 3(10), e1603080.
8. Towns DR, Atkinson IAE, Daugherty CH. Have the harmful effects of introduced rats on islands been exaggerated? Biological Invasions. 2006;8(4):863-91.
9. Veitch CR, Clout MN, Towns DR, (eds). Island Invasives: Eradication and Management. Proceedings of the International Conference on Island Invasives. Gland, Switzerland and Auckland, New Zealand: IUCN; 2011.

The fungi phylum Glomeromycota is essentially unknown by the general public, however behind the scenes these taxa are ubiquitous, one of the most widespread and most important (economically and ecologically) fungal group, despite the small number of species it includes (about 150).  Although many species are not known biologically, all glomeromycotan species are believed to form obligate symbiotic relationships with phototrophs.  Most of these relationships occur (in an enormous diversity of plant species) via formation of “arbuscular mycorrhizal” (AM) associations within the roots, which allow the fungi to use carbohydrates produced by the plant.  In exchange the fungi dramatically increase mineral uptake (phosphorus, in particular) for the plant, essentially extending the plants’ root network with a vast mycorrhiza network. 

Glomeromycotan fungi appear to have low host specificity and a plant might be colonized by multiple species of glomeromycotan species, furthermore, the fungi themselves may form complex underground webs, even indirectly connecting the roots of different species of plants.  Glomeromycota are recorded to significantly impact the growth of most herbaceous plants and tropical trees including almost all human food crops, influence the composition of plant species in plant communities, control pests and fungal pathogens, and ameliorate effects of pollution on plant fitness.  These fungi may be fundamental in sustainable agriculture practices to solve the problem of rapidly depleting rock phosphate reserves, and are relevant to global warming as a significant CO2 sink, receiving and holding fixed carbon in the soil. 

Only very few plants (including less than 20% of existing vascular plants) are known to not form these AM relationships with glomeromycotans.  Some of these are plants in families Brassicaceae (e.g. cabbage, Arabidopsis), Caryophyllaceae (e.g. carnation) and Chenopodiaceae (e.g. spinach).  A small number of glomeromycotan species form other kinds of symbioses, some form external (ectomycorrhizal) associations with trees and shrubs, some form mycorrhizal associations with Asco- or Basidiomycota fungi.  One glomeromycotan (Geosiphon pyriformis), thought to be a primitive representative of the group, forms a symbiosis with cyanobacteria, in which they are the macrosymbiont, housing a consortium of the cyanobacteria in specialized bladders; a relationship possibly representing an ancestral type of symbiosis evolving before terrestrial plant life.   

The Glomeromycota are the oldest known fungi group, found in Ordovician fossils from 460 million years ago, and are hypothesized to have originated 600 million years ago, before the divergence of Asco- Basidiomycota fungi.  Scientists hypothesize these fungi had an important role in the process of early (rootless) land plants colonizing terrestrial habitats. 

The phylum Glomeromycota was created in 2001 as the smallest of the seven currently recognized fungi phyla, representing a very recent understanding of this group.  As late as 1974, glomeromycotan species were all placed in genus Endogone within Zygomycota.  Beginning in the early 2000’s molecular studies uncovered far more diversity at species-, genus- and family-level than traditional morphological characterizations documented (primarily as spore morphologies).  Glomeromycota currently is considered to contain between 150-200 “morphospecies,” however this may well be an underestimate.  Nice descriptions of diversity and evolution of this group can be explored at the Schüßler lab web site. 

(Redecker and Raab 2006; Redecker 2008; Schüßler, Schwarzott and Walker 2001; Wikipedia 2014a, b)

The ocean is a significant influence on Earth’s weather and climate. The ocean covers 70% of the global surface. This great reservoir continuously exchanges heat, moisture, and carbon with the atmosphere, driving our weather patterns and influencing the slow, subtle changes in our climate. The oceans influence climate by absorbing solar radiation and releasing heat needed to drive the atmospheric circulation, by releasing aerosols that influence cloud cover, by emitting most of the water that falls on land as rain, by absorbing carbon dioxide from the atmosphere and storing it for years to millions of years. The oceans absorb much of the solar energy that reaches earth, and thanks to the high heat capacity of water, the oceans can slowly release heat over many months or years.

The oceans store more heat in the uppermost 3 meters (10 feet) that the entire atmosphere, the key to understanding global climate change is inextricably linked to the ocean. Climate is influenced by storage of heat and CARBON DIOXIDE in the ocean, which depends on both physical and biological processes. Let’s look at some of these processes. At the end of the last ice age, about 15,000 years ago, and the ice sheets melted away and climate warmed at that time. Ice sheets began to grow, and climate cool about 130,000 years ago at the beginning of the last ice age. About 130,000 years ago, fed by evaporation of ocean waters, the polar ice caps thickened and expanded Earth cooled by almost 12° C and global sea level to drop 130m below its current level. About 15,000 years ago, this process was reversed as more sunlight reached areas near the Arctic Circle, and Earth emerged from the ice age. Earth is about 8° Celsius (14° Fahrenheit) warmer today than it was then. Still recovering from the ice age, global sea level continues to rise. The past century alone has seen global temperature increase by 0.6 degree Celsius (1 degree Fahrenheit), and the average global sea level over the past decade has risen steadily.

Is this just part of the natural cycle? How much of this warming is due to the burning of fossil fuels? Is human nature affecting Mother Nature? What should we do? Our response to the challenge of global warming begins by formulating the right set of questions. The first step in addressing the issue of global warming is to recognize that the warming pattern, if it continues, will probably not be uniform. The term “global warming” only tells part of the story; our attention should be focused on “global climate change.” The real threat may not be the gradual rise in global temperature and sea level, but the redistribution of heat over the Earth’s surface. Some spots will warm, while others will cool; these changes, and the accompanying shifts in rainfall patterns, could relocate agricultural regions across the planet. By studying the oceans from space, we can unlock a vast store of information about our changing environment.

Climate is affected by both the biological and physical processes of the oceans. In addition, physical and biological processes affect each other creating a complex system. Both the ocean and the atmosphere transport roughly equal amounts of heat from Earth’s equatorial regions – which are intensely heated by the Sun – toward the icy poles, which receive relatively little solar radiation. The atmosphere transports heat through a complex, worldwide pattern of winds; blowing across the sea surface, these winds drive corresponding patterns of ocean currents. But the ocean currents move more slowly than the winds, and have much higher heat storage capacity.

The winds drive ocean circulation transporting warm water to the poles along the sea surface. As the water flows poleward, it releases heat into the atmosphere. In the far North Atlantic, some water sinks to the ocean floor. This water is eventually brought to the surface in many regions by mixing in the ocean, completing the oceanic conveyor belt (see below). Changes in the distribution of heat within the belt are measured on time scales from tens to hundreds of years. While variations close to the ocean surface may induce relatively short-term climate changes, long-term changes in the deep ocean may not be detected for many generations. The ocean is the thermal memory of the climate system.

• Physical characteristics of heat transport and ocean circulation impact the Earth’s climate system. Like a massive ‘flywheel’ that stabilizes the speed of an engine, the vast amounts of heat in the oceans stabilizes the temperature of Earth. The heat capacity of the ocean is much greater than that of the atmosphere or the land. As a result, the ocean slowly warms in the summer, keeping air cool, and it slowly cools in winter, keeping the air warm. A coastal city like San Francisco has a small range of temperature throughout the year, but a mid-continental city like Fargo, ND has a very wide range of temperatures. The ocean carries substantial heat only to the sub-tropics. Poleward of the sub-tropics, the atmosphere carries most of the heat.
• Climate is also influenced by the “biological pump,” a biological process in the ocean that impacts concentrations of carbon dioxide in the atmosphere. The oceanic biological productivity is both a source and sink of carbon dioxide, one of the greenhouse gases that control climate. The “biological pump” happens when phytoplankton convert carbon dioxide and nutrients into carbohydrates (reduced carbon). A little of this carbon sinks to the sea floor, where it is buried in the sediments. It stays buried for perhaps millions of years. Oil is just reduced carbon trapped in sediments from millions of years ago. Through photosynthesis, microscopic plants (phytoplankton) assimilate carbon dioxide and nutrients (e.g., nitrate, phosphate, and silicate) into organic carbon (carbohydrates and protein) and release oxygen.
• Carbon dioxide is also transferred through the air-sea interface. Deep water of the ocean can store carbon dioxide for centuries. Carbon dioxide dissolves in cold water at high latitudes, and is subducted with the water. It stays in the deeper ocean for years to centuries before the water is mixed back to the surface and warmed by the sun. The warm water releases carbon dioxide back to the atmosphere. Thus the conveyor belt described below carries carbon dioxide into the deep ocean. Some (but not all, or even a large part) of this water comes to the surface in the tropical Pacific perhaps 1000 years later, releasing carbon dioxide stored for that period. The physical temperature of the ocean helps regulate the amount of carbon dioxide is released or absorbed into the water. Cold water can dissolve more carbon dioxide than warm water. Temperature of ocean is also impacted the biological pump. Penetrative solar radiation warms the ocean surface causing more carbon dioxide to be released into the atmosphere. Oceanic processes of air-sea gas fluxes effect biological production and consequentially impacting climate. But as plant growth increases, the water gets cloudy and prevents the solar radiation from penetrating beneath the ocean surface.

NASA Oceanography & Climate

NASA satellite observations of the oceans of the past three decades have improved our understanding of global climate change by making global measurements needed for modeling the ocean-atmosphere climate system. NASA uses several instruments to get sea-surface temperature (AVHRR or other), height (altimeter), winds (scatterometers), productivity (MODIS), and salinity (future instruments). Global data sets available on time scales of days to years (and, looking ahead, to decades) have been and will be a vital resource for scientists and policy makers in a wide range of fields. Ocean surface topography and currents, vector winds (both speed and direction), sea-surface temperature, and salinity are the critical variables for understanding the ocean-climate connection.

Sea Winds

Scatterometers are used to measure vector winds. The SeaWinds scatterometer has provided scientists with the most detailed, continuous global view of ocean-surface winds to date, including the detailed structure of hurricanes, wide-driven circulation, and changes in the polar sea-ice masses. Scatterometer signals can penetrate through clouds and haze to measure conditions at the ocean surface, making them the only proven satellite instruments capable of measuring vector winds at sea level day and night, in nearly all weather conditions. Combined with data from Topex/Poseidon, Jason-1, and weather satellites, moorings and drifters, data from SeaWinds and its follow-on missions will be used to study long-term change. Earth’s weather patterns such as El Niño, and the Northern Oscillation, which affect the hydrologic and bio-geochemical balance of the ocean-atmosphere system.

Ocean Surface Topography

Radar altimeters like those on the Topex/Poseidon and Jason missions, are used to measure ocean surface topography. Bouncing radio waves off the ocean surface and timing their return with incredible accuracy, these instruments tell us the distance from the satellite to the sea surface within a few centimeters – the equivalent of sensing the thickness of a dime from a jet flying at 35,000 feet! At the same time, special tracking systems on the satellites give their position relative to the center of mass of Earth also with an accuracy of a few centimeters. By subtracting the height of the satellite above the sea from the height of the satellite above the center of mass, scientists calculate maps of the sea-surface height and changes in the height due to tides, changing currents, heat stored in the ocean, and amount of water in the ocean. By mapping the topography of the ocean we can determine the speed and direction of ocean currents. Just as wind blows around high- and low-pressure centers in the atmosphere, water flows around the high and lows of the ocean surface.

Maps of sea-surface height are most useful when they are converted to topographic maps. To determine topography of the sea-surface, height maps are compared with a gravitational reference map that shows the hills and valleys of a motionless ocean due to variations in the pull of gravity. The GRACE (Gravity Recovery and Climate Experiment) mission will provide very accurate maps of gravity that will allow us to greatly improve our knowledge of ocean circulation. GRACE has provided gravity measurements that are up to 100 times more accurate than previous values. This improved accuracy will lead the way to break-throughs in our understanding of ocean circulation and heat transport. Two animations showing sea surface height (SSH) and sea surface temperature (SST) Anomalies in the Pacific Ocean from October 1992 to August 2002. The increase in temperature and height in the equatorial region west of South America illustrates the 1997-98 El Nino event.

Temperature & Salinity

Water is an enormously efficient heat-sink. Solar heat absorbed by bodies of water during the day, or in the summer, is released at night, or in winter. But the heat in the ocean is also circulating. Temperature & Salinity control the sinking of surface water to the deep ocean, which affects long-term climate change. Such sinking is also a principal mechanism by which the oceans store and transport heat and carbon dioxide. Together, temperature and salinity differences drive a global circulation within the ocean sometimes called the Global Conveyor Belt.

The heat in the water is carried to higher latitudes by ocean currents where it is released into the atmosphere. Water chilled by colder temperatures at high latitudes contracts (thus gets more dense). In some regions where the water is also very salty, such as the far North Atlantic, the water becomes dense enough to sink to the bottom. Mixing in the deep ocean due to winds and tides brings the cold water back to the surface everywhere around the ocean. Some reaches the surface via the global ocean water circulation conveyor belt to complete the cycle. During this circulation of cold and warm water, carbon dioxide is also transported. Cold water absorbs carbon dioxide from the atmosphere, and some sinks deep into the ocean. 

 When deep water comes to the surface in the tropics, it is warmed, and the carbon dioxide is released back to the atmosphere. Salinity can be as important as temperature in determining density of seawater in some regions such as the western tropical Pacific and the far North Atlantic. Rain reduces the salinity, especially in regions of very heavy rain. Some tropical areas get 3,000 to 5,000 millimeters of rain each year. Evaporation increases salinity because as evaporation occurs, salt is left behind thus making surface water denser. Evaporation in the tropics averages 2,000 millimeters per year. This denser saltier water sinks into the ocean contributing to the global circulation patterns and mixing. Ocean salinity measurements have been few and infrequent, and in many places salinity has remained unmeasured. Remotely sensed salinity measurements hold the promise of greatly improving our ocean models. This is the challenge of project Aquarius, a NASA mission scheduled to launch in 2008, which will enable us to further refine our understanding of the ocean-climate connection.

The Biological Pump

Life in the ocean consumes and releases large quantities of carbon dioxide. Across Earth’s oceans, tiny marine plants called phytoplankton use chlorophyll to capture sunlight during photosynthesis and use the energy to produce sugars. Phytoplankton are the basis of the ocean food web, and they play a significant role in Earth’s climate, since they draw down carbon dioxide, a greenhouse gas, at the same rate as land plants. About half of the oxygen we breathe arises from photosynthesis in the ocean.

Because of their role in the ocean’s biological productivity and their impact on climate, scientists want to know how much phytoplankton the oceans contain, where they are located, how their distribution is changing with time, and how much photosynthesis they perform. They gather this information by using satellites to observe chlorophyll as an indicator of the number, or biomass, of phytoplankton cells.

Probably the most important and predominant pigment in the ocean is chlorophyll-α contained in microscopic marine plants known as phytoplankton. Chlorophyll-α absorbs blue and red light and reflects green light. If the ratio of blue to green is low for an area of the ocean surface, then there is more phytoplankton present. This relationship works over a very wide range of concentrations, from less than 0.01 ton early 50 milligrams of chlorophyll per cubic meter of seawater.

The PhyloCode is a formal set of rules governing phylogenetic nomenclature. It is designed to name the parts of the tree of life by explicit reference to phylogeny. The PhyloCode will go into operation in a few years, but the exact date has not yet been determined. It is designed so that it may be used concurrently with the existing codes based on rank-based nomenclature (ICBN, ICZN, etc.). We anticipate that many people whose research concerns phylogeny will find phylogenetic nomenclature advantageous.

The version of the PhyloCode that is posted here is a draft. Some parts of it may change before the code is implemented. Comments are welcome and may be sent to [email protected]. A new version (5), which differs substantially from the one posted here (4c), was approved by the Committee on Phylogenetic Nomenclature in January 2014. It will be posted here once the Preface and Index have been completed. In the meanwhile, a beta version is available on request from Phil Cantino ([email protected]).

The PhyloCode grew out of a workshop at Harvard University in August 1998, where decisions were made about its scope and content. Many of the workshop participants, together with several other people who subsequently joined the project, served as an advisory group (see the PhyloCode preface for a list of the people involved). In April 2000, a draft was made public on this web site and comments were solicited from the scientific community. All comments were forwarded to the advisory group, and many of them elicited discussion. A second workshop was held at Yale University in July 2002, at which the discussion focused on the governance of species names and the publication of a book of phylogenetically defined clade names as a companion to the PhyloCode (see the History section of the Preface).

The First International Phylogenetic Nomenclature Meeting, which took place July 6–9, 2004 in Paris, was attended by about 70 systematic and evolutionary biologists from 11 nations. The program can be downloaded from the “Events” page. This was the first open, multi-day conference that focused entirely on phylogenetic nomenclature, and it provided the venue for the inauguration of the International Society for Phylogenetic Nomenclature (ISPN). The ISPN membership elects the Committee on Phylogenetic Nomenclature (CPN), the responsibilities of which are explained in Art. 22 of the PhyloCode. The CPN has taken over the role of the advisory group that oversaw the earlier stages of development of the PhyloCode.

The Third International Phylogenetic Nomenclature Meeting was held July 21–23, 2008 at Dalhousie University, Halifax. More information can be downloaded from the “Events” page.

The International Society for Phylogenetic Nomenclature is open to all. More information about the ISPN and a membership form can be found at http://phylonames.org.

Changes in Version 4. The current version of the PhyloCode (version 4c), which was posted in January 2010, differs from version 4b in many minor ways, which are detailed in the Preface. In contrast, version 4b (posted in September 2007) differs in major ways from version 3. See the “Changes in Version 4” section of the Preface for details.

Most reef-building corals contain photosynthetic algae, called zooxanthellae, that live in their tissues. The corals and algae have a mutualistic relationship. The coral provides the algae with a protected environment and compounds they need for photosynthesis. In return, the algae produce oxygen and help the coral to remove wastes. Most importantly, zooxanthellae supply the coral with glucose, glycerol, and amino acids, which are the products of photosynthesis. The coral uses these products to make proteins, fats, and carbohydrates, and produce calcium carbonate (Barnes, R.D., 1987; Barnes, R.S.K. and Hughes, 1999; Lalli and Parsons, 1995; Levinton, 1995; Sumich, 1996).

 The relationship between the algae and coral polyp facilitates a tight recycling of nutrients in nutrient-poor tropical waters. In fact, as much as 90 percent of the organic material photosynthetically produced by the zooxanthellae is transferred to the host coral tissue (Sumich, 1996). This is the driving force behind the growth and productivity of coral reefs (Barnes, 1987; Levinton, 1995).

In addition to providing corals with essential nutrients, zooxanthellae are responsible for the unique and beautiful colors of many stony corals. Sometimes when corals become physically stressed, the polyps expel their algal cells and the colony takes on a stark white appearance. This is commonly described as “coral bleaching” (Barnes, R.S.K. and Hughes, 1999; Lalli and Parsons, 1995). If the polyps go for too long without zooxanthellae, coral bleaching can result in the coral’s death.

Because of their intimate relationship with zooxanthellae, reef-building corals respond to the environment like plants. Because their algal cells need light for photosynthesis, reef corals require clear water. For this reason they are generally found only in waters with small amounts of suspended material, i.e., in water of low turbidity and low productivity. This leads to an interesting paradox—coral reefs require clear, nutrient-poor water, but they are among the most productive and diverse marine environments (Barnes, 1987).

symbioses
Sponges form symbiotic relationships with various organisms, including mutualisms with photosynthetic bacteria/plant cells, and swimming scallops and crabs, and parasitisms on mollusc shells.

NOTE “symbiosis” is a general term used in North America for any two organisms living together. There are several categories of symbiosis described in the scientific literature, but the one most commonly used, commensalism (one partner benefits while the other is unaffected) assumes information about the participants that is usually unavailable. The two symbioses of clearest definition (and most interest) are mutualism, where both partners benefit, and parasitism, where one partner benefits and the other is harmed.

Mutualism

Several west-coast sponges house single-celled plants known as zoochlorellae. The relationship is thought to be mutualistic in that the plants provide products of photosynthesis (glycerol, glucose, amino acids) to the host in return for a place to stay, and the host provides carbon dioxide and ammonia nutrients required for photosynthesis. A common host for zoochlorellae is the “crumb-of-bread” sponge Halichondria panicea which has two growth forms. One is a flat, tough open-coast form that often contains so many zoochlorellae that it appears greenish in colour.

For some reason, the green open-coast Halichondria often has a bad smell. Whether this has something to do with its algal symbionts, or with the presence of defensive chemicals, is not known.

The other form is often found on docks in quiet water conditions, although may occur in open-coast situations. It has a softer consistency and mostly lacks symbionts.

NOTE thought to be similar to green plant cells found in west-coast sea anemones. These are discussed elsewhere in the ODYSSEY: SEA ANEMONES: SYMBIONTS.

What is the explanation for the enhanced growth performance of the nudibranch? Select the best idea from the list below and  see explanations of the answers. Ideas from Knowlton & Highsmith 2005 J Exper Mar Biol Ecol 327: 36.

Nudibranchs eat more of the zoochlorella-containing sponge.

The symbionts increase the density of the sponge tissue; hence, providing more tissue per bite for the nudibranch.

The symbionts increase the nutritional content of the food.

Introduction

Russulaceae is one of the largest families of ectomycorrhizal fungi that plays a dominant role in many vegetations worldwide. The core of this family consists of two genera, Lactarius and Russula, both described from Europe two centuries ago as clearly recognizable agaricoid genera. However, recent research (Buyck et al., 2008) demonstrated that the traditional classification of Russulaceae into these two genera is not supported. Instead, the family consists of four mainly agaricoid genera and includes some corticioid species. In one of these genera (Multifurca), some rare representatives of the former Lactarius and Russula are united. The rest of Russula is supported as a monophyletic group. Lactarius, notwithstanding its striking feature of exuding milk or latex (thus: the milkcaps) which always seemed a good synapomorphic character, is paraphyletic and is split in two genera: Lactarius and Lactifluus.

Based on morphological and molecular characteristics, Lactifluus seems the most variable out of the four Russulaceae genera. Lactifluus mainly consists of tropical species and recent studies discovered large cryptic diversity within the genus (Stubbe et al., 2010; Van de Putte et al., 2010). Morphologically, this genus is characterized by the complete absence of zonate and viscose to glutinose caps, and it contains many species with veiled and velvety caps and all known annulate species (Buyck et al., 2008). Lactarius on the other hand, has a more temperate distribution, with many cold-adapted species and contains the typical zonate and viscid to glutinose milkcaps. Our present knowledge results in a large genus Lactarius with about 75% of the milkcaps and a smaller genus Lactifluus, but the real number of species in Lactifluus might be higher due to cryptic diversity, which seems to be absent in Lactarius. Our hypothesis is that Lactifluus evolved genetically faster but is morphologically more stable, while morphological variation is more common in the genetically slower evolving genus Lactarius. The speciation-extinction dynamics of both genera are clearly different. These discrepancies have strongly influenced the evolutionary history of both genera. 

Objectives and approach

In current phylogenies, the genus Lactifluus is strongly underrepresented. We want to meet this deficit by collecting more species of this genus. Recent biodiversity studies and expeditions to unexplored areas provided surprising new insights into the phylogeny of Lactifluus (e.g. Van de Putte et al., 2009). Previous research indicated that many valuable sites are highly endangered remnants of original forest. Some of these sites are protected and studied by the Center for Tropical Forest Science (CTFS, part of the Smithsonian Tropical Research Institute). One important benefit of CTFS woodlands is that all tree species are inventoried, so the ectomycorrhizal trees are known, which makes targeted searches possible. We plan expeditions to such selected areas, for searching phylogenetic relevant material (missing links) and to contribute to an inventory of the biodiversity. This might also contribute to the protection of these relict areas, as prioritizing habitats for conservation often relies on estimation of species richness and endemism (Bickford et al., 2007).
A phylogeny of Russulaceae, focusing strongly on Lactifluus, will be constructed based on the following nuclear and mitochondrial genes: nLSU (nuclear ribosomal large subunit 28S region), tef1 (codes for the translation elongation factor 1α), rpb1 and rpb2 (code for the largest and second largest subunit of the RNA polymerase II gene) and mSSU (mitochondrial ribosomal small subunit 16S region).

• Constructing a comprehensive phylogeny is a first step towards obtaining insight into any existing phylogenetic predispositions to certain morphological and ecological character states within these genera. In this second step we will use phylogenies to address general trends and broad historical patterns in the evolution of Russulaceae. We will collect and integrate existing data concerning distribution, morphology and ecology of the different species. Subsequently, computational techniques will be used to study the correlation of the collected data and to compare the evolution of the Lactarius and Lactifluus diversity through time. These phylogenetic comparative analyses will be carried out with the use of stochastic mapping techniques, applying Bayesian approaches. First of all we will check if, besides the L. gerardii and L. volemus species complexes, L. piperatus and L. gymnocarpoides are also cryptic species complexes with a large genetic diversity, and whether cryptic speciation is thus a widespread phenomenon in Lactifluus. The diversification consequences of particular character states will be explored by testing key-innovative hypotheses, in which stochastic models of character evolution and cladogenesis are employed, integrated into a Bayesian framework in which uncertainty in historical inferences (such as phylogenetic relationships) is allowed (Ree, 2005). With these tests we can investigate whether or not a morphological novelty or a switch in host plant family results in a different rate of speciation. We will assess directionality in character state transformations using ancestral state reconstruction methods, and we will investigate the possible correlation of characters (Schmitt et al., 2009). The outcome of these techniques can provide an idea on how the ancestor of Lactarius and Lactifluus may have looked like and how their morphological and ecological characters have evolved. Russulaceae is an ideal model group to apply these new techniques to, because these techniques require comprehensive phylogenies, which will be available for the four genera (Lactarius and Lactifluus in Ghent, Russula and Multifurca in Paris). Furthermore it is a group which apparently unites genera with a very different evolutionary history, a world-wide distribution, host plant specialists and generalists.

References

Bickford D., Lohman D.J., Sodhi N.S., Ng P.K.L., Meier R., Winker K., Ingram K.K. & Das I. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22(3): 148–155.

Buyck B., Hofstetter V., Eberhardt U., Verbeken A. & Kauff F. (2008). Walking the thin line between Russula and Lactarius: the dilemma of Russula sect. Ochricompactae. Fungal Diversity 28: 15–40.

Hibbett D.S. & Matheny P.B. (2009). The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses. BMC Biology 7: 13.

Matheny P.B., Aime M.C., Bougher N.L., Buyck B., Desjardin D.E., Horak E., Kropp B.R., Lodge D.J., Soytong K., Trappe J.M. & Hibbett D.S. (2009). Out of the Palaeotropics? Historical biogeography and diversification of the cosmopolitan ectomycorrhizal mushroom family Inocybaceae. Journal of Biogeography 36: 577–592.

Otálora M.A.G., Martínez I., Aragón G. & Molina M.C. (2010). Phylogeography and divergence date estimates of a lichen species complex with a disjunct distribution pattern. American Journal of Botany 97(2): 216–223.

Ree R.H. (2005). Detecting the historical signature of key innovations using Stochastic models of character evolution and cladogenesis. Evolution 59(2): 257–265.

Schmitt I., del Prado R., Grube M. & Lumbsch H.T. (2009). Repeated evolution of closed fruiting bodies is linked to ascoma development in the largest group of lichenized fungi (Lecanoromycetes, Ascomycota). Molecular Phylogenetics and Evolution 52: 34–44.

Stubbe D., Nuytinck J. & Verbeken A. (2010). Critical assessment of the Lactarius gerardii species complex (Russulales). Fungal Biology 114(2-3): 271–283.

Van De Putte K., De Kesel A., Nuytinck J. & Verbeken A. (2009). A new Lactarius species from Togo with an isolated position. Cryptogamie Mycologie 30(1): 1–6.

Van De Putte K., Nuytinck J., Stubbe D., Le H.T. & Verbeken M. (2010). Lactarius volemus sensu lato (Russulales) from northern Thailand: morphological and phylogenetic species concepts explored. Fungal diversity 45(1): 99–130.

Abstract

The genus Cistus comprises a group of about 20 shrub species found in wide areas throughout the whole
Mediterranean region to the Caucasus. Being one of the main constituents of the Mediterranean-type maquis, this
plant genus is peculiar in that it has developed a range of specific adaptations to resist summer drought and frequent
disturbance events, such as fire and grazing. In addition, it can form both ectomycorrhizas and arbuscular mycorrhizas. In this paper, we review the information available on the ectomycorrhizal fungi of Cistus across its entire
geographic range, as gathered and critically sifted from both published literature sources and personal observations. Although the resulting data matrix was based primarily on accounts of sporocarp inventories in the field, existing knowledge of the features of Cistus natural and synthesized ectomycorrhizas was also included and discussed. In total, more than 200 fungal species belonging to 40 genera have been reported so far to be associated with
Cistus. An analysis of the pattern of ectomycorrhizal diversity and host specificity revealed that members of the
Cortinariaceae and Russulaceae make the most of both Cistus-aspecific and Cistus-specific mycobionts. Further
studies are needed to expand our preliminary knowledge of the mycorrhizal ecology and biology of Cistus and its
fungal associates, focusing on topics such as mycobiont diversity, host specificity, fungal succession, mycorrhizal
influence on stress tolerance, and impact of disturbances, while comparing the findings with those from other
ecosystems.

Introduction

Although Europe and adjacent areas are relatively wellknown from the mycological point of view, some ecosystems have received comparatively little attention,especially concerning the role played by mycorrhizal symbiosis. In particular, given the ecological importance of host specificity for plant ectotrophic communities and the
associated mycota, studies describing the specificity patterns occurring in selected ecosystems are of premium
significance, as they can contribute to a better definition of the environmental biotic and abiotic factors that affect
specificity phenomena, and how the specialization of ectomycorrhizal fungi and plant hosts originated and
evolved (Molina et al. 1992; Erland and Taylor 2002; Van der Heijden and Sanders 2002). A significant example
of these “neglected mycorrhizal niches” is the Cistusdominated maquis. Cistus harbors a group of about 20
woody, evergreen or semi-deciduous shrub species found in wide semi-arid areas from Madeira and the Canary
Islands throughout the whole Mediterranean region to the Caucasus (Arrington and Kubitzki 2003). Some species,
such as C. carthaginensis in Spain (Boscaiu and Guemes 2001), have a very limited or even punctiform range and
are severely threatened of extinction.

Cistus species have evolved specific adaptations to resist severe summer
drought stress and to regenerate rapidly after fire, a key ecological factor influencing the evolution and dynamics of
the Mediterranean vegetation. Thanks to their ability as early colonizers after disturbance, Cistus species often
form pure stands in vast areas heavily subjected to fire and/or grazing (for an extensive bibliography on various
aspects of Cistus ecology and biology, see (http://www.cistuspage.org.uk).Cistus may form both ectomycorrhizas and vesicular arbuscular mycorrhizas, the other widespread type of mycorrhizal association (Smith and Read 1997). Although most plant species form only one type of association, the dual mycorrhizal status is not unique of Cistus, but is also present in Populus, Salix, Alnus, and Eucalyptus (Smith and Read 1997), and also in some tropical tree genera such as the myrtaceous Ixora, Syzygium, and Tristania (Reddell et al. 1996; Moyerson et al. 2001). In these hosts,
ectomycorrhizas and arbuscular mycorrhizas can either co-occur at a comparable level in the root system or one
type can be predominant, but it is not yet clear which factors favour dominance by each functional association.
In the case of Cistus and Eucalyptus, both genera inhabiting fire-susceptible ecosystems, it has been suggested that mycorrhizal plasticity may represent an important adaptive trait to the cyclical pattern of accumulation and loss of organic resources due to fire (Smith and Read 1997). At variance with the cistaceous host genus Helianthemum (Yu et al. 2001), no reports of ectendomycorrhizas formation by Cistus species are known to date.To expand current knowledge of mycorrhizal biology of Cistus, a new research program at our institution is focusing on the isolation and full characterization of the ectomycorrhizas formed by the fungal symbionts exclusively or prevalently associated with Cistus spp. (Nuytinck et al. 2004; Rinaldi and Comandini, unpublished observations). While screening published data on Cistus mycorrhizas to select suitable candidates for ectomycorrhizal characterization, we were struck by the fact that information on Cistus-associated mycota is generally widely dispersed in the mycological literature, and no recent
comprehensive accounts exist on the topic. In the present review paper, we attempt to fill this gap by providing an
updated checklist of fungal species reported to establish ectomycorrhizas on Cistus spp. on the basis of field
observations. The cases where the association has been confirmed experimentally, either through direct observation of naturally occurring or synthesized mycorrhizas, and by molecular approaches, have been highlighted. We also
attempt to discuss the ecological significance of Cistus mycorrhizas in relation to what is known on the role played
by ectomycorrhizal diversity in other better-studied ecosystems. Finally, we indicate those we believe are the
main research needs to fully disclose Cistus mycorrhizal ecology.

When more than one host genus was mentioned in the original reference, for example “under Quercus and
Cistus”, or “in Quercus stands with Cistus understory”, the relevant fungal species was generally not considered as
a Cistus symbiont, unless this particular association was confirmed by other sources. When more than one Cistus
species was present, the relevant mycobiont(s) was assigned to all potential hosts. Evidence from studies on
the morpho-anatomical and molecular characterization of ectomycorrhizas formed by taxonomically diverse fungal
species on Cistus spp. were also inserted in the data set, as they support hypotheses from field observations. In
addition to studies concerning naturally-occurring, fieldcollected mycorrhizas, data coming from synthesized
mycorrhizas were also considered.

Despite all efforts to cover as large a number of bibliographic sources as possible, our literature survey
was clearly partial and incomplete, and a number of valuable records may have been missed. However, we are
confident that the assembled data matrix includes the majority of the ecologically relevant information available
on Cistus-associated fungal species, especially when Cistus-specific mycobionts are concerned. As the vast
majority of the data set consists of field observations of sporocarps rather than associations confirmed by direct
inspection of ectomycorrhizas, the limitations inherent to data sources must be emphasized. Indeed, the reports of
putative mycorrhizal relationships based solely on sporocarp associations are obviously subject to an unquantifiable degree of error. Trappe (1962) has explained the criteria that should lead to the exclusion or inclusion of
literature reports when compiling lists of mycorrhizal associations based on sporocarp observations. In compiling
the data set for this study, we strictly observed these guidelines and, also on the basis of our personal experience, discarded or labeled all spurious and/or dubious records. As regards synthesized ectomycorrhizas, it should
be stressed that associations induced in laboratory experiments may not occur under field conditions (Harley and
Smith 1983; Molina et al. 1992). Finally, the identification of some fungi in the references we have considered may
not be correct.

Collecting the data

Data on the association between Cistus spp. and ectomycorrhiza-forming fungi presented in this paper are overwhelmingly based on reports of field observations of sporocarp associations with potential hosts. The data set
contains both information collated from a variety of published sources, including taxonomic monographs of
specific groups of ectomycorrhizal fungal genera and the few previous surveys of fungi associated with Cistus, and
personal collections and observations. Fungal taxa belonging to genera for which the mycorrhizal status is currently
uncertain were not listed. Only records clearly mentioning (potential) Cistus hosts were included in the data matrix

crispus, incanus, ladanifer (often mentioned under the synonym ladaniferus), laurifolius, monspeliensis, populifolius, salvifolius] are explicitly reported in the literature to form specific associations. Most fungal records are referred to common host species occurring over large geographic areas (C. incanus, C. monspeliensis, C.salvifolius), and few records are available for rare or uncommon species such as C. clusii, C. crispus, and C. populifolius.

In most cases, the potential host species was not indicated in the original reference, probably due to the
rather homogeneous morphology of the species within the genus Cistus, with subsequent identification problems for
non-specialists, and to the common occurrence of several Cistus species growing tightly together in a stand, whicmade it difficult, if not impossible, to specify the plant partner in a number of instances. Geographically, the
largest number of records were originally collected in Spain, followed by peninsular and insular Italy and
southern France, and a few in Morocco. Virtually no information is available for other extended regions in North
Africa (e.g., Tunisia and Algeria) and for the eastern side of the Cistus range, i.e., the Balkans, the Aegean Archipelago,
the coasts of Anatolia, the Caucasus, Syria, Lebanon. In Israel, studies on the mycorrhizal status of naturally
occurring C. incanus and C. villosus have been conducted(Litav 1965; Berliner et al. 1986), although the involved
fungal taxa were not identified.

In general, all the larger and ecologically key ectomycorrhizal fungal genera harbor a significant number of
species that are associated with Cistus. Cortinarius (29 species) and Russula (28) are the best represented in the
list, followed by Inocybe (23), Amanita (22), Hygrophorus(13), Lactarius (12, excluding the probable spurious report
of L. deliciosus, see below), Hebeloma (12), Boletus (10),Tuber (10, excluding T. californicum), Tricholoma (10). At
the family level, Cortinariaceae (for a comment on the concept of families in the Agaricales, see notes in Table 1)
and Russulaceae, clearly form the prevalent groups. The association of Cistus with numerous hypogeous ascomycetes (Table 1) seems to be a common feature of the Cistaceae as a whole, as other genera, such as Helianthemum, also show similar mycorrhizal preferences (e.g., Malloch and Thorn 1985).

“Broad host range” fungi, which can form mycorrhizal with host plants from diverse plant families, orders, and
even classes (Molina et al. 1992), occur frequently in the list, and include Amanita vaginata, Hebeloma crustuliniforme, Paxillus involutus, Telephora terrestris, and Tricholoma sulphureum. Many other listed fungal species
are more frequently associated with Quercus spp., and their association with Cistus, when reliably identified, is
probably sporadic and/or occasional. These include, for example, several of the Lactarius species reported here,
such as L. atlanticus, L. chrysorrheus, L. ilicis, L. mairei,and L. zonarius (Basso 1999). However, these records are
important because they provide valuable information concerning the mycorrhizal ecology of selected fungal
species, revealing their tendency to switch hosts when

Diversity and host specificity of Cistus ectomycorrhizal fungi

Current knowledge about Cistus ectomycorrhizal fungal diversity is based mostly on above-ground observations of
fungal fruitbodies (Table 1). About 230 fungal species belonging to 40 genera are listed, belonging to both
Ascomycota and Basidiomycota, a number of Cistus associates considerably larger than previous accounts
(Malloch and Thorn 1985; Lavorato 1991; Ballero et al. 1992; Vila and Llimona 1999, 2002). Early studies
reviewing ectomycorrhizal fungi and relevant plant hosts overlooked Cistus and its mycoflora (e.g., Trappe 1962),
partly due to a focus on forests rather than shrublands. On the plant side, nine different Cistus species [albidus, clusii,

these share the same environment—a feature that has certainly played a major role in the evolution of host
specificity among ectomycorrhizal fungi—and broaden our perspective of Cistus-compatible fungi.
The analysis of the assemblage of the fungal taxa more closely linked to Cistus also reveals an interesting pattern.
Two different groups of mycorrhizal fungi can be discerned here. The first comprises “narrow host range” fungi, i.e.,
fungal species forming mycorrhizas only in association with a single plant genus (Molina et al. 1992), Cistus in this
case. About 35 Cistus-specific fungi are identifiable to date, all of them being epigeous basidiomycetes. These
include Leccinum corsicum, Amanita cistetorum, Hebeloma album, H. cavipes, H. cistophilum, H. erumpens,
Inocybe cistobulbipes, I. rocabrunae, Hygrophorus pseudodiscoideus var. cistophilus, Lactarius cistophilus, L.
cyanopus, L. tesquorum, Russula cistoadelpha, R. monspeliensis, R. tyrrhenica, and a number of Cortinarius
species. Again, a few genera within the Cortinariaceae and,on a minor scale, Russulaceae, seem to comprise almost all
the fungal species highly specialized to Cistus. A second group has those fungal species which although not
associated exclusively with Cistus, commonly establishfunctional symbiosis with this host, and are often a
component of the macromycetous fungal flora in Cistusdominated plant communities. Tuber melanosporum, Amanita muscaria, Hebeloma hiemale, Laccaria laccata fo.pseudobicolor, and L. proxima belong to this group.
Among the macromycetes putatively linked to Cistus spp., it is apparent that some of the claimed associations are
very unlikely. This is the case, for example, of the related Suillus collinitus and Rhizopogon spp., both genera being
currently accepted as specific to conifers (almost exclusively Pinaceae) (Kretzer et al. 1996; Molina et al. 1999).
Also Amphinema byssoides has been reported as being restricted to coniferous tree species (Erland and Taylor
1999). Another clear example of a most likely spurious report is that of the common Pinus-associated Lactarius
deliciosus from Greece (Zervakis et al. 1998) and Spain (Ortega and Esteve-Raventós 1999). It is, thus, possible
that some fungi in the list are in reality not compatible with Cistus, but rather with other hosts present in the same
community, most frequently Quercus spp. (see above) and Pinus spp. The absence of Cenococcum in Table 1 is also
noticeable, as this symbiont is almost ubiquitous on the roots of most ectomycorrhizal hosts in a range of ecological
situations (LoBuglio 1999). Given the little attention devoted so far to the observation of Cistus ectomycorrhizal
morphotypes (see below), however, it cannot be excluded that Cenococcum forms mycorrhizas with Cistus.
In spite of the fairly large number of ectomycorrhizal macromycetes linked to Cistus spp. in Mediterranean-type
ecosystems, information on the features of relevant mycorrhizas is remarkably limited. To date, only very
few accounts of Cistus ectomycorrhizal types exist in the literature. Most studies focused on the ectomycorrhizas
formed by hypogeous ascomycetes, such as Tuber and Terfezia with Cistus spp., both under natural and cultured
conditions. These investigations resulted in the full

characterization of the ectomycorrhizas formed by Tuber spp. on C. incanus (Fontana and Giovannetti 1979;
Giovannetti and Fontana 1982), and in several other preliminary and/or not exhaustive descriptions of mycorrhizal morpho-anatomical details (Chevalier et al. 1975; Fusconi 1983; Leduc et al. 1986; Wenkart et al. 2001;
Roth-Bejerano et al. 2003). For basidiomycetes, descriptions of the mycorrhizas formed by L. laccata and Boletus
rhodoxanthus on C. ladanifer (Torres et al. 1995; Hahn 2001), by Hebeloma sacchariolens on C. salvifolius
(Rosell 1981) and, more recently, by Lactarius tesquorum on Cistus sp. (Nuytinck et al. 2004), are available.
Common host-dependent features of all the ectomycorrhizal types described so far on Cistus spp. are (for the
specific terminology used to characterize ectomycorrhizae, see Agerer 1986, 1987–1998, 1991): simple or monopodial-pinnate ramification systems; small diameter of ectomycorrhizal tips; thin mantle thickness; cortical cells
generally present in two rows, tangentially rectangular, either radially rectangular orientated or square to radially
rectangular orientated; Hartig net generally uniseriate, surrounding one–two rows of cortical cells and rarely
reaching the endodermis (“cortical Hartig net”, for a description of this peculiar structure, see Smith and Read
1997).

In addition to the ectomycorrhizal types mentioned above, very recent observations of Cistus roots excavated
in Sardinia (Italy) have led to the isolation of ectomycorrhizas of Lactarius cistophilus and of a morphotype
unequivocally formed by a sebacinoid mycobiont (Rinaldi and Comandini, unpublished observations). The latter
finding adds to the increasing evidence that members of the Sebacinaceae, a family assigned to the heterobasidiomycetous order Auriculariales, are common symbionts in various ectomycorrhizal communities. Typical ectomycorrhizas formed by these fungi have been recently detected by both molecular and morphological analyses on several temperate deciduous and coniferous trees, including Carpinus, Corylus, Fagus, Tilia, Picea, and Abies (Selosse
et al. 2002; Urban et al. 2003; Comandini, unpublished observations), and also in Australian Eucalyptus Mediterranean-type forests (Glen et al. 2002).

In recent years, the application of a range of molecular tools has greatly enhanced our knowledge of ectomycorrhizal communities, expanding well beyond classic morphotyping our possibilities to track and identify ectomycorrhizas and to compare the above- and belowground mycorrhizal fungal components of ecosystems (Horton and Bruns 2001). Unfortunately, this “revolution” has only marginally impacted research on Cistus ectomycorrhizas. To date, indeed, only the mycorrhizas of Lactarius tesquorum on Cistus sp. have been fully characterized from both a molecular and morphological point of view (Nuytinck et al. 2004). Clearly, the confirmation of many putative Cistus mycobionts and the unambiguous identification of their mycorrhizas await a more general recourse to molecular methods.

Comparing ectomycorrhizal diversity in different ecosystems

In addition to forming extensive patches of pure shrublands, Cistus is also a significant presence in other
vegetation communities. These communities include the mixed Mediterranean maquis or garrigue, where Cistus
occurs together with other sclerophyllous (not-ectomycorrhizal) scrubs, such as Olea, Phyllirea, Pistacia, Erica,
Arbutus, and some Quercus and Pinus-dominated communities, where Cistus is an element of the undercanopy
vegetation and colonizes clearings and open areas. The data gathered in this study indicate that the number of
ectomycorrhizal fungal species associated with Cistus is significant, and support the importance of this symbiosis in
these Mediterranean ecosystems. On the other hand, when compared to other better-known host plants such as
Pseudotsuga menziesii, which associates with some 2000 fungal species in North America (Trappe 1977), the
ectomycorrhizal diversity of Cistus might look rather poor.However, it should be stressed that comparing lists of
fungal associates drafted by different authors might be biased to some extent by personal choices for inclusion or
exclusion of those fungal genera for which the mycorrhizal status is uncertain or not fully confirmed. Focusing on the
information available for other better-studied Mediterranean-type ecosystems, some 660 fungal associates, many
of which are endemic, have been recorded for Eucalyptus in natural environments of Australia (Castellano and
Bougher 1994; Bougher 1995). Eucalyptus is also believed to have the potential to associate with the richest flora of
host genus-specific ectomycorrhizal fungi in the world (Molina et al. 1992), while diversity in its plantations is
considerably lower in both Australian and exotic areas (Lu et al. 1998a,b; Giachini et al. 2000) (an extensive account
of Eucalyptus ectomycorrhizal fungi can be found at http://www.ffp.csiro.au/research/mycorrhiza/eucfungi.html). Eucalyptus and Cistus share a small contingent of associated fungi, included in the genera Pisolithus, Scleroderma, and Laccaria, with the characteristics of “early stage” species.These mycobionts appear in the early phases of fungal
successions and represent, in some cases, pioneer fungi,being often typical of disturbed habitats with young trees
and shrubs, or may occur even in freshly cleared areas and often associate with a diversity of hosts. Some Hebeloma
listed in Table 1 are also well known early stage fungi.

What needs to be done

Our knowledge of Cistus mycorrhizal ecology is too limited to draw any simple conclusions for this host plant
and its associated fungi as for many key aspects mentioned above. However, information acquired from studies of
other ecosystems may help to highlight priority areas for future research. In particular, the pattern and role of host
specificity, possibly for each fungal species, in Cistus ectomycorrhizal communities should be investigated, as
the importance of host specificity in other ectomycorrhizal communities has been underlined (Bruns et al. 2002).

Examining the plant-fungal associations for Cistus would also serve to elucidate mycobiont–host distribution and
mycobiont–host species relationships (Newton and Haigh 1998), to see if they have a general validity or, and
eventually how, they change in specialized environments.Many of the Cistus-specific symbionts listed here, e.g.,
Cortinarius spp. and Inocybe spp., have been identified only very recently, which highlights the need for in-depth
taxonomical surveys of these and other fungal genera in Cistus maquis over the entire host geographic range.
Belowground ectomycorrhizal diversity in Cistus natural communities should also be explored to see if it reflects the
Cortinariaceae and Russulaceae dominance detected aboveground, and the morphological and molecular
characterization of the prevailing ectomycorrhizal types should be performed.

Work aimed at confirming the identity of putative mycobionts and extending their number would certainly be
easier if carried out in pure Cistus stands, rather than in areas where it grows mixed with other ectomycorrhizal
hosts. However, the exploration of diversity and biology of Cistus mycorrhizas in mixed plant communities could
provide key information on the structure of both the plant and fungal components of these communities in Mediterranean-type ecosystems. Doubtlessly, molecular tools will play a major role in tackling these complex issues. As data on the succession of mycorrhizal fungi in Cistus ecosystems are totally lacking, community level studies should
also be conducted to address this important aspect, as well as the impact of mycorrhizal colonization upon the fitness
of Cistus and its resilience to natural and anthropogenic disturbances, such as strong water limitation, fire, overcutting, and grazing.

Considering the ecological niches occupied by Cistus and the intermediate position of this host genus in the
vegetation series leading to evergreen Quercus or Pinus climax forests on one side, and to impoverished pastures
and/or desertified lands on the other, a deeper knowledge of Cistus ectomycorrhizal fungal communities may well
prove to be of wider significance and to contribute to understand the role and dynamics of mycorrhizas in inherently unstable ecosystems, especially if integrated into broader ecological investigations. These studies may also provide valuable tools to help shape future programs of protection and management of natural resources in vast
areas across the Mediterranean basin. In general, Cistus holds the potential to develop into an alternative model to
assess the role of mycorrhizal symbiosis in ecosystem functioning of Mediterranean-climate shrublands throughout the world. Clearly, we are just at the beginning of this research journey.

 Introduction

In the Federal Register of August 13, 1998 (63 FR 43402) (FDA 1998), the FDA announced the availability of a new document entitled “Accidental Radioactive Contamination of Human Food and Animal Feeds: Recommendations to State and Local Agencies” (hereinafter 1998 FDA document) replacing an earlier 1982 FDA document (FDA 1982). The 1998 FDA document provides guidance to State and local agencies to aid in emergency response planning and execution of protective actions associated with the production, processing, distribution, and use of human food and animal feeds accidentally contaminated, e.g., due to a nuclear power plant accident, with radioactive elements called radionuclides. In addition, the 1998 FDA document provides broader and more current information regarding radionuclides in food than the 1982 FDA document.

FDA has adopted guidance levels for radionuclide activity concentration established in the 1998 FDA document in a Compliance Policy Guide (CPG) entitled “Guidance Levels for Radionuclides in Domestic and Imported Foods.” The CPG rescinds and replaces guidance levels for radionuclide activity concentration in food offered for import established in current CPG Sec. 560.750 Radionuclides in Imported Foods — Levels of Concern (CPG 7119.14) with guidance levels established in the 1998 FDA document. FDA has also adopted these same guidance levels for radionuclide activity concentration for domestic food in interstate commerce. Additionally, the FDA has expanded its policy from food accidentally contaminated with radionuclides to food accidentally or intentionally contaminated with radionuclides. The 1998 FDA document remains unaffected by the issuance of the CPG.

FDA uses guidance levels for radionuclide activity concentration in food to help determine whether domestic food in interstate commerce or food offered for import into the United States presents a safety concern. The purpose of this supporting document is to present information taken from the 1998 FDA document that explains the basis for the guidance levels in the CPG and how these guidance levels differ from guidance levels established in 1986, which have been superseded.

Protective Action Guides

The calculation of guidance levels for radionuclide activity concentration in food depends in part on Protective Action Guides (PAGs). PAGs are radiation dose levels to an individual at which protective action should be considered to limit the radiation dose to that individual. PAGs were previously defined in the1982 FDA document as “projected dose commitment values to individuals in the general population that warrant protective action following a release of radioactive material.” In this context, the phrase “dose commitment” refers to the radiation dose received by an individual. The PAGs contained in the 1982 FDA document were developed from the prevailing scientific understanding of the relative risks associated with radiation as described in the 1960 and 1961 reports of the Federal Radiation Council (FRC 1960, 1961). The 1982 FDA guidance document established two levels for PAGs. The lower level, called the Preventative PAG, was a projected dose commitment of 5 mSv to the whole body, active bone marrow, or any other organ except the thyroid, or a projected dose commitment of 15 mSv to the thyroid. The upper level, called the Emergency PAG, was a projected dose commitment of 50 mSv to the whole body, active bone marrow, or any other organ except the thyroid, or a projected dose commitment of 150 mSv to the thyroid.

The 1998 FDA document redefined a PAG as the “committed effective dose equivalent⁽¹⁾ or committed dose equivalent⁽²⁾ to an individual organ or tissue that warrants protective action following a release of radionuclides.” The 1998 FDA document replaced the Preventative and Emergency PAGs with one set of PAGs for the ingestion pathway. The PAGs established in the 1998 FDA document are 5 mSv for committed effective dose equivalent or 50 mSv committed dose equivalent to an individual tissue or organ, whichever is more limiting (i.e., the most limiting PAG results in the lowest level of radionuclide activity concentration in food).

For 5 mSv committed effective dose equivalent (the PAG adopted in the new CPG), the associated lifetime total cancer mortality would be 2.25 x 10^-4 or approximately 1 in 4400. For comparison, the estimate of the normal lifetime total cancer mortality in the United States for the general population, not associated with additional radiation dose from ingestion of food contaminated with radionuclides, is 0.19 or approximately 1 in 5 (CIRRPC 1992). Thus, in a general population of 10,000 individuals, the number of cancer deaths over the lifetime of the individuals would be 1990; if each received a committed effective dose equivalent of 5 mSv, the number of cancer deaths over the lifetime of the individuals could increase in theory by about 2, for a total of 1992 cancer deaths.

The numerical estimate of cancer deaths presented above for the recommended PAG of 5 mSv was obtained by the practice of linear extrapolation from the nominal risk estimate for lifetime total cancer mortality for the general population at 100 mSv dose equivalent in the whole body.⁽³⁾ Other methods of extrapolation to the low-dose region could yield higher or lower numerical estimates of cancer deaths. Studies of human populations exposed at low doses are inadequate to demonstrate the actual magnitude of risk. There is scientific uncertainty about cancer risk in the low-dose region below the range of epidemiological observation, and the possibility of no risk cannot be excluded (CIRRPC 1992).

The term “PAG” is used by FDA and other Federal and state agencies. International organizations use the term “intervention level of dose” (ICRP 1984b). The PAGs established in the 1998 FDA document and adopted in this supporting document are the same as the intervention levels of dose used by international organizations. The 1998 FDA guidance and this supporting document retain use of the term “PAG” for consistency with other U.S. Federal and state agencies.

FDA’s Guidance Levels for Radionuclide Activity Concentrations in Food Established in 1986

Following the Chernobyl nuclear accident in 1986, FDA that same year issued CPG Sec. 560.750 Radionuclides in Imported Foods — Levels of Concern (CPG 7119.14) which established guidance levels referred to as Levels of Concern (LOCs) for radionuclide activity concentration in food offered for import.

The LOCs in CPG 7119.14 were derived from the Preventative PAGs established in the 1982 FDA guidance document and were based on the following assumptions: 1) the entire intake of food would be contaminated, 2) Iodine-131 would be a major source of radiation dose for only 60 days following the accident, and 3) Cesium-134 + Cesium-137 could be a major source of radiation dose for up to one year. The LOCs provided such a large margin of safety that derivation of LOCs for other radionuclides, judged to be of less health significance, was considered unnecessary. The LOCs in CPG 7119.14, established in 1986, are given in Table 1.

FDA’s 1998 Guidance Levels for Radionuclide Activity Concentration in Food Adopted in the CPG

The guidance levels for radionuclide activity concentration in food in the CPG are referred to in the 1998 document as “Derived Intervention Levels” or DILs. DILs are used by scientists internationally to describe the radionuclide activity concentrations at which introduction of protective measures should be considered. The term DILs as used in the CPG replaces the term LOCs used in CPG 7119.14 and allows for consistency in scientific terminology between the CPG and the internationally accepted scientific term. Efforts by international organizations to develop DILs have been extensive. Derivations have been based on consensus values for the intervention levels of dose, called PAGs by FDA, and have been used to establish guidance levels for radionuclides in foods within individual countries and in international trade. In general, food with concentrations below the DILs is permitted to move in international trade without restriction. Food with concentrations at or above the DILs is not normally permitted into international trade.⁽⁴⁾

By definition, a DIL corresponds to the radionuclide activity concentration in food present throughout the relevant period of time that, in the absence of any intervention, could lead to an individual receiving a radiation dose equal to the PAG. The equation given below is the formula that the agency used for calculating recommended DILs.

DILs (Bq/kg) = [PAG (mSv)] / [f x FI (kg) x DC (mSv/Bq)]

Where:

DC = Dose Coefficient; the radiation dose received per unit of radionuclide activity ingested (mSv/Bq)

f = Fraction of the food intake assumed to be contaminated

FI = Food Intake; the quantity of food consumed in an appropriate period of time (kg)

Guidance levels or LOCs contained in CPG 7119.14 addressed only I-131, Cs-134 and Cs-137 because these radionuclides were known at that time to be the principal radionuclides that contribute to radiation dose by ingestion following a nuclear reactor accident. Information gained following the Chernobyl accident determined that Ru-103 and Ru-106 could also contribute to radiation dose and, therefore, these radionuclides were included in the 1998 FDA document. In addition, other radionuclides were included in the 1998 FDA document to address other radiological emergencies where there is a possibility of accidental radioactive contamination of food. This approach provides the flexibility necessary to respond to special circumstances that may be unique to a particular accident. The types of accidents and the principle radionuclides for which DILs were developed are:

• Nuclear reactors (I-131; Cs-134 + Cs-137; Ru-103 + Ru-106)
• Nuclear fuel processing plants (St-90; Cs-137; Pu-238 + Pu-239 + Am-241)
• Nuclear waste storage facilities (Sr-90; Cs-137; Pu-238 + Pu-239 + Am-241)
• Nuclear weapons (i.e., dispersal of nuclear weapon material without nuclear detonation) (Pu-239), and
• Radioisotope thermoelectric generators and radioisotope heater units are used in space vehicles (Pu-238).

The DILs are for radionuclides expected to deliver the major portion of the radiation dose from ingestion during the first year following an accidental episode of radiological food contamination. If there is concern that food will continue to be significantly contaminated beyond the first year, the long-term circumstances need to be evaluated to determine whether the recommended DILs would be appropriate or if other guidance is more applicable.

Detailed information on derivation of DILs is presented in the appendix. The DILs are based upon calculations for nine radionuclides expected to be the predominant contributors to radiation dose through ingestion (Sr-90, I-131, Cs-134, Cs-137, Ru-103, Ru-106, Pu-238, Pu-239, and Am-241). For each radionuclide, DILs were calculated for six age groups using PAGs, dose coefficients relevant to each radionuclide and age group, and dietary intakes relevant to each age group. The age groups include 3 months, 1 year, 5 years, 10 years, 15 years and adult (>17 years). The dose coefficients were adopted by FDA from the International Commission on Radiological Protection Publication 56 (ICRP 1989). The dietary intakes were derived from a 1984 EPA report which presented average daily food intake by age and gender (EPA 1984a, EPA 1984b).

The nine radionuclides listed above comprise five radionuclide groups, each having common characteristics. The five groups are: Strontium-90; Iodine-131; Cesium-134 + Cesium-137; Ruthenium-103 + Ruthenium-106; and Plutonium-238 + Plutonium-239 + Americium-241. An accident could involve more than one of the five groups. A single DIL for each radionuclide group was chosen based on the most limiting PAG and age group for the radionuclide group (i.e., the most limiting PAG and age group result in the lowest DIL). These five DILs are the ones incorporated into the new CPG.

The calculations underlying the DILs are based on the entire diet for each age group, not for individual foods or food groups. Unlike the previous LOCs that assumed 100 percent radionuclide contamination of the diet, DILs assume ten percent radionuclide contamination of the diet which is then multiplied by a factor of three. Use of ten percent of the dietary intake as the portion contaminated is consistent with recommendations made by a group of experts to the Commission of the European Communities (CEC 1986b) and by the Nuclear Energy Agency (NEA) of the Organization for Economic Cooperation and Development (NEA 1989). FDA applied an additional factor of three to account for limited sub-populations that might be more dependent on specific food supplies. Therefore, a value of thirty percent is the fraction of food intake that FDA presumed to be contaminated. For infants, (i.e., the 3-months and 1-year age groups) DILs were calculated assuming 100 percent radionuclide contamination of the infant diet.

With one exception (LOCs for I-131 in non-infant food), guidance levels or DILs for radionuclides established in the 1998 FDA document that FDA has adopted in the CPG are higher than guidance levels or LOCs for those same radionuclides contained in the CPG 7119.14. In deriving guidance levels or DILs contained in the 1998 FDA document, FDA employed updated international consensus values for intervention levels of dose (called PAGs by FDA) as well as updated dose coefficients and food intake estimates. In addition, information gained by FDA and others following the Chernobyl accident determined that the amount of food affected by an accident would be significantly lower than the level originally estimated. For this reason, DILs contained in the 1998 FDA document assume thirty percent of the dietary intake would be contaminated after a nuclear accident, compared to the 100 percent assumption of contamination employed in deriving LOCs. FDA’s decision to reduce the assumption for dietary intake contamination from 100 percent to thirty percent is the main reason that the guidance levels established in the 1998 FDA document and adopted in the CPG are higher than the guidance levels contained in CPG 7119.14.

The 1998 FDA document established guidance levels only for food accidentally contaminated with radionuclides in domestic interstate commerce. In the CPG, FDA has adopted those same guidance levels for food either accidentally or intentionally contaminated with radionuclides, regardless of whether that food is in domestic interstate commerce or offered for import. FDA has taken this action because radionuclides that could be implicated in an event involving the accidental contamination of food could also be implicated in an event involving the intentional contamination of food. The radionuclides addressed in the 1998 FDA document are widely used and available. Furthermore, an incident resulting in release of radionuclides from one of the nuclear facilities addressed in the 1998 FDA document would likely result in the release of the same radionuclides regardless of whether the cause of the release was accidental or intentional. FDA has therefore concluded that the assumptions used in establishing the DILs in the 1998 FDA document and adopted in the CPG are appropriate for both accidental as well as intentional radionuclide contamination of food.

The DILs established in the 1998 FDA document and contained in the CPG for food offered for import and food in domestic interstate commerce are given in Table 2.

Appendix — Derivation of Recommended Derived Intervention Levels

The Derived Intervention Level (DIL) for a specific radionuclide is calculated as follows:

DILs (Bq/kg) = [PAG (mSv)] / [f x FI (kg) x DC (mSv/Bq)]

Where:

DC = Dose Coefficient; the radiation dose received per unit of radionuclide activity ingested (mSv/Bq)

f = Fraction of the food intake assumed to be contaminated

FI = Food Intake; the quantity of food consumed in an appropriate period of time (kg)

The Protective Action Guides (PAGs) used are 5 mSv committed effective dose equivalent, or 50 mSv committed dose equivalent to individual tissues and organs, whichever is more limiting.

Dose coefficients (DCs) are given in Table 3 and food intakes are given in Tables 4 and 5. The fraction of food intake assumed to be contaminated (f) equals 0.3, except for I-131 in infant diets where f equals 1.0.

Radionuclides

Based upon data on radionuclides in human food following the Chernobyl accident, DILs for I-131, Cs-134, Cs-137, Ru-103 and Ru-106 would apply following incidents involving nuclear reactors. For incidents at nuclear fuel reprocessing facilities and nuclear waste storage facilities, DILs for Sr-90, Cs-137, Pu-239, and Am-241 would apply. For nuclear weapons incidents and incidents involving radioisotope thermal generators (RTGs) and radioisotope heater units (RHUs) used in space vehicles, DILs for Pu-239 and Pu-238, respectively, would apply. The selection of these radionuclides as the major contributors to radiation dose through ingestion is consistent with recommendations on DILs published by NEA, WHO, CODEX, and CEC (NEA 1989, WHO 1988, CODEX 1989, CEC 1989a, IAEA 1994).

Age Groups and Dose Coefficients (DCs)

The general population was divided into six age groups ranging from infants to adults and corresponding to the age groups in ICRP Publication 56 (ICRP 1989) for which ICRP has published DCs. The age groups are 3 months, 1 year, 5 years, 10 years, 15 years, and adult. The radionuclides, age groups and dose coefficients used in the calculations are presented in Table 3.

 Food Intake

Food intake included all dietary components including tap water used for drinking, and is the overall quantity consumed in one year, with exceptions in the period of time for I-131 (T_1/2 = 8.04 days) and Ru-103 (T_1/2 = 39.3 days). For these radionuclides, the quantities consumed were for a 60-day period and a 280-day period, respectively, due to the more rapid decay of these radionuclides. The intake periods for I-131 and Ru-103 are the nearest whole number of days for decay of these radionuclides to less than 1% of the initial activities.

Dietary intakes were derived from a 1984 EPA report which presented average daily food intake by age and gender (EPA 1984a, EPA 1984b). The EPA intakes were based on data from the 1977-1978 Nationwide Food Consumption Survey published by the U. S. Department of Agriculture (USDA 1982, USDA 1983). The age groups and annual dietary intakes for various food classes and the total, calculated from data in the EPA report, are given in Table 4. The dietary intakes derived for the ICRP age groups for which DCs are available, using the results in Table 4, are presented in Table 5.

 Fractions of Food Intake Assumed to be Contaminated

For food consumed by most members of the general public, ten percent of the dietary intakes was assumed to be contaminated. This assumption recognizes the ready availability of uncontaminated food from unaffected areas of the United States or through importation from other countries, and also that many factors could reduce or eliminate contamination of local food by the time it reaches the market.

Use of ten percent of the dietary intake as the portion contaminated was consistent with recommendations made by a Group of Experts to the Commission of the European Communities (CEC 1986a) and by the Nuclear Energy Agency (NEA) of the Organization for Economic Cooperation and Development (NEA 1989). The NEA noted that modification of this value would be appropriate if justified by detailed local findings.

FDA applied an additional factor of three to account for the fact that sub-populations might be more dependent on local food supplies. Therefore, during the immediate period after a nuclear accident, a value of 0.3 (i.e., thirty percent) is the fraction of food intake presumed to be contaminated. If, subsequently, there is convincing local information that the actual fraction of food intake that is contaminated (f) is considerably higher or lower, there will be adequate time to determine whether to adjust the value of f (and therefore adjust the values of the DILs) for the affected area.

For infants, (i.e., the 3-months and 1-year age groups) the diet consists of a high percentage of milk and the entire milk intake of some infants over a short period of time might come from supplies directly impacted by an accident. Therefore, f was set equal to 1.0 (100%) for the infant diet.

Selection of Recommended Derived Intervention Levels

DILs are presented in Table 6 for Sr-90, I-131, Cs-134, Cs-137, Ru-103, Ru-106, Pu-238, Pu-239, and Am-241 for six population age groups and applicable PAGs. Two criteria were used in selecting a single DIL for each radionuclide for inclusion in the new CPG.

First, the most limiting DIL for either of the applicable PAGs was selected for each of the nine radionuclides. These DILs are presented in Table 7 for each of the six age groups. In addition, the average DIL is presented for the radionuclide group Pu + Am, composed of Pu-238, Pu-239, and Am-241, and the radionuclide group Cs, composed of Cs-134 + Cs-137. The three radionuclides in the Pu + Am group deposit on the bone surface and are alpha-particle emitters. The radionuclides in the Cs group are deposited throughout the body and are beta-particle and gamma-ray emitters. The average values are used for these groups because the calculated DILs for radionuclides in each group are similar.

The radionuclides Ru-103 and Ru-106 are chemically identical, are deposited throughout the body, and are beta-particle and gamma-ray emitters. However, their widely differing half lives (i.e., 39.3 days and 373 days, respectively) result in markedly differing individual DILs which do not permit simple averaging. Instead, the concentrations of Ru-103 (C3) and Ru-106 (C6) are divided by their respective DILs and are then summed. The DIL for the Ruthenium group is set at less than one.

Therefore, [(C3) / (DIL3)] + [(C6) / (DIL6)] < 1.0   (equation 1)

This assures that the sum of the separate radiation dose contributions from the Ru-103 and Ru-106 concentrations will be less than that contemplated by the Protective Action Guide during the first year after an accident.

Second, there are dietary components which are common to all six age groups. A principal example is fresh milk, for which the consumer of particular supplies cannot be identified in advance. Therefore, the most limiting DIL for all age groups in Table 7, for each radionuclide or radionuclide group, was selected and is applicable to all components of the diet.

These DILs are presented in Table 8 and were rounded to two significant figures (one significant figure for the Pu + Am group). These are the DILs adopted in the new CPG. The DILs in Table 8 apply independently to each radionuclide or radionuclide group, because they apply to different types of incidents, or in the case of a nuclear reactor incident, to different limiting age groups. However, the DILs for Ru-103 and Ru-106 are used in equation 1 to evaluate that criterion for the radionuclide group Ru-103 + Ru-106. The DILs in Table 8 are given in Table 2 in the main text.