Carbon sequestration in boreal forests: below-ground interactions matter

K. E. Clemmensen, A. Bahr, O. Ovaskainen, A. Dahlberg, A. Ekblad, H. Wallander, J. Stenlid, R. D. Finlay, D. A. Wardle, B. D. Lindahl. Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest. 2013. Science. Vol. 339 no. 6127 pp. 1615-1618. DOI:10.1126/science.1231923 

One of the most important developments in plant ecology over the last 20 or so years is the inclusion of belowground interactions with fungi into traditional studies of plant diversity, productivity, and ecosystem functions. Results like those from van der Heijden (1998)--which showed experimentally that the assumed link between ecosystem function and plant diversity was actually driven by arbuscular mycorrhizal fungal diversity (through their effects on plant communities)—must alter how we see plant community dynamics. Not only does this reinforce the importance of complexity in ecology, but more specifically it suggests that if fungi are a necessary component of plant community identity and function, they must be explicitly considered in management and conservation plans.

For example, an important current issue is the question of which ecosystems will be carbon sinks as part of a focus on atmospheric CO2 levels. Understanding the mechanisms by which carbon is stored is therefore an important topic. Boreal forests sequester net amounts of carbon in soil and it is generally assumed that this is as a result of plant litter and organic matter accumulating in soil. Clemmensen et al. (2013) examined soil chronosequences for forested islands in Sweden to test whether this hypothesis held. These islands differed in the frequency of fire occurrences, between large and frequently burnt islands and smaller, infrequently burnt islands.

The authors identified the age since fixation of C found in the chronosequences and used models of C source to look at the relative contribution of the two possible processes: either fixation of C through aboveground plant litter or below-ground inputs through root-associated fungi. Carbon input tended to be higher on the small islands that were burnt less often, and this was associated entirely with root-derived input. Further, DNA barcoding showed that on these small islands, there were mycorrhizal fungi associated with the soil depths where the root-derived inputs were occurring. On islands which burned more frequently, and had lower carbon input, fungi were absent at these depths (figure below). This difference in fungal profile was related to the fact that infrequently burnt islands had older mycelium with low turnover, hence greater carbon sequestration.

From Clemmensen et al (2013). A) Fungal functional groups associated with soil depths on large, frequently burnt islands (panel 1) and small, infrequently burnt islands (panel 2).

The authors convincingly show that, at least in some ecosystems, the view that decomposition of litter primarily drives humus accumulation (and the accompanying carbon sequestration) must be tempered with the knowledge that organic layers also accumulate from below by roots and root-associated fungi. This suggests that there is a need to consider fungal communities as well as plant communities for when managing forests and making inventories of global carbon stores. And probably a need to consider fungi much more often in general.

Evolution on an ecological scale

Andrew Gonzalez, Ophélie Ronce, Regis Ferriere, and Michael E. Hochberg. 2013. Evolutionary rescue: an emerging focus at the intersection between ecology and evolution. Philos Trans R Soc Lond B Biol Sci. 368 (1610).doi: 10.1098/rstb.2012.0404 (Intro to special issue).

David A. Vasseur, Priyanga Amarasekare, Volker H. W. Rudolf, Jonathan M. Levine. 2011. Eco-Evolutionary Dynamics Enable Coexistence via Neighbor-Dependent Selection. The American Naturalist, Vol. 178, No. 5, pp.E96-E109.

Ecology and evolution are often treated as connected but ultimately discrete areas of study. Ecological processes are usually the main source of explanation for ecological patterns and  ecologists may ignore evolutionary processes under the assumption that these are most important over longer time scales than are of interest (e.g. speciation). However, there is also an increasing recognition that rapid evolutionary dynamics can contribute to ecological observations. In a time where rapid changes to climate and habitat are the greatest threats to most species, the suggestion that rapid evolution might play a role in extinction prevention and diversity maintenance is an important one.

Increasingly researchers are exploring this concept. The concept of evolutionary rescue (ER), has been particularly championed by Andy Gonzalez and Graham Bell of McGill University. ER results when evolution occurs fast enough to arrest population declines and allow populations to avoid extinction in the face of changing conditions. Changing conditions resulting in maladapted populations should result in population declines followed by extinction. However, if selection for resistant types (which are present in the population, or result from mutations) occurs, population declines can be countered. The result is a characteristic u-shape curve, showing the initial geometric decline, followed by a geometric increase – escape from extinction is then a balance between rates of evolution and success of resistant types compared to rates of population decline.

From Bell & Gonzalez 2009.

The question of whether evolution may have relevance to population declines is not precisely new, but it is especially relevant given we are in a period of habitat changes and extinction. A special issue of Proc B is focused only ER, on the question of its importance, prevalence, and predictability. Many of the articles extend theory, exploring assumptions about the type of environmental change, type and extent of the threat, presence of dispersal, spatial gradients, etc. A few articles attempt the more difficult task of testing for ER in natural systems and assessing its likely prevalence and value to conservation activities. It is an interesting journal issue and a great example of the importance of context in determining when an idea takes off. The theoretical background for evolutionary rescue has existed for many years, but it took the context of climate change (and perhaps the collaboration of an ecologist and evolutionary biologist?) for it to gain ground as an area of ecological research.

Another interesting paper, this one linking evolutionary dynamics with community coexistence, is from Vasseur et al. (2011). In this case, the authors suggest an evolutionary mechanism that could augment coexistence when ecological conditions allow for niche partitioning and that could allow coexistence when ecological conditions lead to competitive exclusion. If species exhibit tradeoffs between traits that are optimal for intraspecific interactions and traits that are optimal for interspecific interactions, evo-ecological dynamics can produce coexistence. Such tradeoff means that a species will be a superior interspecific competitor when rare and a poor interspecific competitor when common. Such a tradeoff creates neatly alternately selective pressures depending on whether a species is common (fitness declines) or rare (fitness increases). This is presented as a theoretical model, but it seems like in a tractable system one could easily test for changes in ecological and evolutionary pressures as predicted by the model.

No one would argue with the conclusion that a closer relationship between ecology and evolutionary biology would be beneficial for both. But in practice this seems to be the exception rather than the rule. "Evolutionary ecology" as it exists is fairly restricted, and if complaints about seminar topics is to provide a hint, most ecologists feel disconnected from evolutionary topics and vice versa. If evolutionary dynamics are relevant on an ecological scale, it seems that we should at least attempt to understand their prevalence and importance in natural systems.

NSF funds Project Baseline

NSF approved 1.2 million dollars for a unique and visionary idea: collect 12 million seeds and store them in seed banks for years to come. And while storing seeds for the future doesn't sounds so different from what other groups have already done, where Project Baseline differs is that this seed bank is not only a conservation measure--preserving natural genetic variation from plant populations for the future--but also an opportunity to track the effects of changing climate on the direction and rate of evolution in these species.

This idea was first explored in "The Resurrection Initiative: Storing Ancestral Genotypes to Capture Evolution in Action" (Franks et al 2007). By collecting and storing seeds from both within and across populations throughout the range of a species, ancestral and descendent populations can be compared in the not too distant future. The role of adaptive evolution and range shifts can be explored through this lens. Project Baseline is a great example of how much we can learn from long-term, collaborative experiments and projects (other examples include NutNet , NCEAS), and how valuable funding such projects should be considered.

Trend in ecology, 2010

Sciences are always in a state of ebb and flow (sorry), and topics of study fall in or out of fashion in response to paradigms shifts, methodological advances, and to support necessary ecological applications.
For the sake of curiosity, I've compiled the top keywords from ecology publications in 2010. Obviously there are many covariates, but it should come as no surprise that the top words were "biodiversity" (667 times), "climate change" (293), and "conservation" (274); other popular keywords were "evolution" (277), "population (ecology)" (273), and the rather vague "patterns" (196).

(click image for larger view)

The sushi of tomorrow… Jellyfish rolls?

With the world’s fisheries teetering on the edge of collapse, familiar items at your local sushi bar might disappear in the near future. One candidate for replacing the Hamachi, Ikura, Maguru, Tai, and Toro on the menu is the jellyfish, which seems to be doing well – too well, actually – in today’s environment.

In recent years, jellyfish outbreaks have become more frequent and more severe. These outbreaks can have lasting ecological and economic consequences. They can wreak havoc on the tourist industry by closing beaches and harming swimmers, cause power outages by blocking cooling intakes at coastal power plants, reduce commercial fish abundance via competition and predation, spread fish parasites, burst fishing nets, and contaminate catches.

A review by Anthony Richardson and his collaborators suggests that human activities such as overfishing, eutrophication, climate change, translocation, and habitat modification have dramatically increased jellyfish numbers. Their research, which was published this week in Trends in Ecology and Evolution, highlights that the structure of pelagic ecosystems can abruptly transition from one that is dominated by fish to one that is dominated by jellyfish.

Richardson and his collaborators present a potential mechanism to explain how local jellyfish aggregations can spread, displace fish, and form an alternative stable state to fish-dominated ecosystems. Jellyfish are like the opportunistic weed of the sea, giving them an edge in environments stressed by climate change, eutrophication, and overfishing. In these disturbed environments, the abundance of jellyfish relative to filter-feeding fish increases until a tipping point is reached. Under normal conditions, filter-feeding fish keep jellyfish populations in check via competition for planktonic food and (perhaps) predation on an early life-stage of the jellyfish. At the tipping point, jellyfish numbers are such that they begin to overwhelm any control of their vulnerable life-cycle stages by fish predators. At the same time, jellyfish progressively eliminate competitors and predators via their predation on fish eggs and larvae. As jellyfish abundance increases, sexual reproduction becomes more efficient, allowing them to infest new habitats where fish might have formally controlled jellyfish numbers.

Richardson and his collaborators suggest that one way to hit the brakes on what they call the “the never-ending jellyfish joyride” is to harvest more jellyfish for human consumption. Jellyfish have been eaten for more than 1000 years in China, where they are often added to salads. In Japan they are served as sushi and in Thailand they are turned into a crunchy noodle concoction. Although the taste and texture of jellyfish might not be appealing to some westerners, I for one have yet to meet a sushi that I didn’t like. Of course, jellyfish harvesting is unlikely to return systems to their fish-dominated state if the stresses that caused the ecosystem shift remain.

Richardson, A. J., A. Bakun, G. C. Hays, and M. J. Gibbons. 2009. The jellyfish joyride: Causes, consequences and management responses to a more gelatinous future. Trends in Ecology and Evolution, 24 (6), 312-322 DOI: 10.1016/j.tree.2009.01.010

Fire and the changing world

This is probably the most appropriate blog I have ever written. My family and I were evacuated two weeks ago because of the Jesusita fire in Santa Barbara, and several homes in our neighborhood were lost. Here in Santa Barbara we have experienced multiple years of extremely large fires, with this last one occurring much earlier than previous fires.

Wildfires have been a part of the Earth’s biota likely since organisms first died and dried on land. Ecosystems have been shaped by fire, numerous organisms have evolved strategies to cope with fire and human cultural development has close tied to fire. In a recent review paper in Science by David Bowman, Jennifer Balch and colleagues, they asked the question: how have fires changed and what does the future look like? Human activities are changing fire patterns and climate change may be entering a feedback with fire. Global warming has been linked to increases in extreme fire weather, making large, destructive fires more probable. However, these large fires feedback into this loop because they release compounds that have strong greenhouse effects. Further, smoke plumes inhibit cloud formation, reinforcing the dry conditions that lead to the fires in the first place.

They argue that fire needs to be incorporating into models of climate change and especially those that link ecosystem properties climate change. Fire may change the distribution of specific habitat types beyond that predicting by responses to climate change alone.

Bowman, D., Balch, J., Artaxo, P., Bond, W., Carlson, J., Cochrane, M., D'Antonio, C., DeFries, R., Doyle, J., Harrison, S., Johnston, F., Keeley, J., Krawchuk, M., Kull, C., Marston, J., Moritz, M., Prentice, I., Roos, C., Scott, A., Swetnam, T., van der Werf, G., & Pyne, S. (2009). Fire in the Earth System Science, 324 (5926), 481-484 DOI: 10.1126/science.1163886

Hurricanes might contribute to global warming

In a large-scale study published this week in Proceedings of the National Academy of Sciences, Hongcheng Zeng and colleagues show that hurricane damage can diminish a forest’s ability to absorb carbon dioxide from the atmosphere. Their results suggest that an increase in hurricane frequency due to global warming may further amplify global warming.

The annual amount of carbon dioxide a forest absorbs from the atmosphere is determined by the ratio of tree growth to tree mortality each year. When hurricanes cause extensive tree mortality, not only are there fewer trees in the forest to absorb greenhouse gases, but these tree die-offs also emit carbon dioxide, thus potentially warming the climate.

Using field measurements, satellite image analyses, and empirical models to evaluate forest and carbon cycle impacts of hurricanes, the researchers established that an average of 97 million trees have been affected each year for the past 150 years over the continental United States, resulting in a 53-million ton annual biomass loss and an average carbon release of 25 million tons per year. Over the period of 1980–1990, released CO2 potentially offset carbon absorption by forest trees by 9–18% over the entire United States. Impacts on forests were primarily located in Gulf Coast areas such as southern Texas, Louisiana, and Florida, but significant impacts also occurred in eastern North Carolina.

These results have important implications for evaluating positive feedback loops between global warming and environmental change.


Zenga, H., J. Q. Chambers, R. I. Negrón-Juárez, G. C. Hurtt, D. B. Baker, and M. D. Powell. (2009). Impacts of tropical cyclones on U.S. forest tree mortality and carbon flux from 1851 to 2000. PNAS, 106 (19), 7888-7892. DOI:10.1073/pnas.0808914106

Climate change increases West Nile Virus outbreaks in the U.S.

According to a study recently published in Environmental Health Perspectives, climate change has increased the prevalence of West Nile Virus infections in the United States. In one of the largest surveys of West Nile Virus cases to date, the authors find a correlation between increasing temperature and rainfall and outbreaks of the mosquito-borne disease between 2001 and 2005. Because warming weather patterns and increasing rainfall are both projected to accelerate with global warming, the authors predict that climate change will exacerbate West Nile Virus outbreaks in the future.

In the study, Dr. Jonathan Soverow and his collaborators matched more than 16,000 confirmed West Nile cases in 17 states to local meteorological data.

Warmer temperatures had the greatest effect on outbreaks. By extending the length of the mosquito breeding season and decreasing the amount of time it takes mosquitoes to reach their adult, biting stage, warmer weather means more biting mosquitoes longer. Moreover, increasing temperature speeds multiplication of the virus within insects, so mosquitoes in warmer climates have a greater viral load, making them more likely to infect humans.

Increased precipitation was also correlated with higher rates of West Nile Virus infection. A single, heavy rainstorm resulting in two or more inches of rain increased infection rates by 33%, while smaller storms had less of an effect on infection rates. Heavier rainfall events can increase disease prevalence by creating pools of water in which mosquitoes can breed and by increasing humidity, which stimulates mosquitoes to bite and breed. Total weekly rainfall had a smaller but significant effect on West Nile Virus infections, with an increase of 0.75 inch of rain/week increasing the number of infections by about 5%.

Warmer, wetter weather patterns might expand the niches of the mosquito species that carry West Nile Virus. In California, for instance, several mosquito species carrying the West Nile Virus have extended their ranges into higher elevations and coastal areas as temperatures have warmed. Changing weather patterns might also affect certain species of birds that are reservoirs for West Nile Virus. For example, droughts can push bird populations into urban areas, making West Nile Virus outbreaks in human populations more likely.

Soverow, J.E., G.A. Wellenius, D.N. Fisman, and M.A. Mittleman. 2009. Infectious disease in a warming world: How weather influenced West Nile Virus in the United States (2001-2005). Environmental Health Perspectives. Online 16 March 2009 DOI: 10.1289/ehp.0800487

Salamaders and climate change -impending extinctions?

By the now the evidence of a global frog decline, perhaps even an extinction crisis, has been well documented. But what about salamanders? They are normally less abundant and less-studied compared to frogs, but is there evidence of the same general pattern of declining population sizes? According to Sean Rovito and colleagues, the answer is unfortunately yes. They repeated a plethodontid (lungless) salamander survey done in the 1970’s in Central America and found that many species have declined. In fact they failed to find a couple of previously very abundant species. They also found that species declines were phylogenetically non-random and so these declines may result in the loss of whole clades of species, meaning that the evolutionary history of these salamanders is at risk.

The authors attempted to determine the cause of these declines and found that neither habitat loss or the chytridiomycosis fungal disease implicated in other declines explained these salamander declines. The authors hypothesize that these declines are a direct result of climate change –namely changing temperature and humidity. If so, we may be witnessing some of the first extinctions that are directly caused by climate change.

S. M. Rovito, G. Parra-Olea, C. R. Vasquez-Almazan, T. J. Papenfuss, D. B. Wake (2009). Dramatic declines in neotropical salamander populations are an important part of the global amphibian crisis Proceedings of the National Academy of Sciences, 106 (9), 3231-3236 DOI: 10.1073/pnas.0813051106

Post script:
We had a comment questioning the use of climate change as an explanation and here is my response.

Science works by finding parsimonious explanations, until through experimentation or observation another, better explanation emerges. The previous explanations of habitat loss or fungal infections were not supported. These habitats, known as cloud forests, are very humid. The lungless salamanders have no lungs and instead breath through their skin, which must be kept moist. These forest are becoming drier, hence the probable connection. Here's a quote from the paper:

"Pounds et al. (25) used modeling to show that largescale warming led to a greater decrease in relative humidity at Monteverde compared to that caused by deforestation. Species of cloud forest salamanders that can still be found rely at least
in part on bromeliads. Bromeliads depend on cloud water deposition and are predicted to be articularly vulnerable to climate change (26, 27)."

Doesn't sound like "magic" to me, rather a robust hypothesized mechanism worthy of more testing. Given that species are going extinct, it is important to suggest likely mechanisms, providing an impetus for more research.

For those that think that scientists use climate change as boogey man to scare up more research funding (i.e., Crichton), please read the science. You'll discover honest, hardworking folks that are trying to understand this changing world and whose research can only benefit you , me and the salamanders.