Getting to the Roots (and Fungi) of Carbon Sequestration

This week, I found a paper that I’m calling the best of both worlds. Well, for me at least. This paper combines my past (and lingering) interest in island biogeography with a current interest in climate change and carbon storage.

If you have been reading my blog long enough then you already know my love of islands. They are just so darn useful. In the past, I have focused on oceanic islands, but lake islands are also really neat. These types of islands typically form when lower lying land areas fill with water, effectively cutting off higher areas from the mainland and making them into islands. As such, these islands usually already contain forest as opposed to an oceanic island that emerges from the ocean and must be colonized. A new study, published in journal Science, looks at a fire-driven boreal forest chronosequence on forested lake islands in northern Sweden. Such a chronosequence allows the study of soil carbon sequestration over time scales of centuries to millennia.

This new study looks at roots and their associated fungi (mycorrhizae) as sources of this stored carbon. I’m not going to spend the space to describe mycorrhize, but will, instead, send you over to my Free Market Fungi post for more information, if you need it. It is known that 16 percent of the global carbon stock is sequestered in soils. To date, most carbon studies of this type focus on aboveground leaf litter as the fundamental determinants of this carbon accumulation. But a large portion of photosynthetically fixed carbon is actually directed belowground to the roots and, subsequently, the mycorrhizae. Now, let’s add fire. It has been shown that when a forest doesn't burn, the soil and ecosystem carbon accumulate unabated, and in a linear fashion. Add this information together and it becomes a big deal when it comes to correctly allocating carbon, calculating the long term sequestration rates, and predicting how forests will respond to climate change and other environmental shifts.

The study sites were in two adjacent lakes, Lake Hornavan and Lake Uddjaure, in northern Sweden. The islands in these lakes were formed after the most recent glaciation and come in a variety of sizes. In terms of fire, larger islands burn more frequently because they are larger targets for lightning strikes. As a result, several of the large islands in these lakes have burned in the last century, whereas some of the small islands haven’t burned in at least 5000 years. This lack of fire leads to very thick humus layers (or organic layers towards the top of the soil column) on smaller islands, up to 1 meter thick!

The researchers divided islands into three size classes of 10 islands each: large (over 1 ha), medium (0.1-1.0 ha), and small (less than 0.1 ha). They took soil samples from these islands to look at the organic soil profiles and found that large islands accumulated 6.2 kg of C per square meter belowground with a mean time since fire of 585 years, medium islands accumulated 11.2 kg of C per square meter with a mean time since fire of 2180 years, and small islands 22.5 kg of C per square meter with a mean time since fire of 3250 years. Then they looked at the carbon dynamics across this chronosequence by analyzing bomb 14C. This allowed them to determine the age since fixation of soil carbon. Then they fitted a mathematical model to measurements of carbon mass and age distribution across the soil profiles for six of the islands (3 large, 3 small). This model revealed that the distribution of carbon mass and age could only be predicted when they included carbon from roots. This root-derived carbon accumulation was found to be larger on small islands (70 percent, that's a LOT!) than large islands (47 percent). They were able to explain the entire carbon sequestration difference on small islands from these root-derived inputs. The model also showed that small islands store a major proportion of their soil carbon in the deeper soil layers, those over 100 years old. However, below 20 cm depth, the root-derived carbon inputs were shown to be low and to decompose slowly. So the root-derived carbon input into the upper layers probably contributes to the long-term buildup of humus that is seen on these islands. But, as usual, that's not the end of the story.

We know that fungi play very important roles in forest ecosystems, both as decomposers and in root-assoicated carbon transport and respiration. So the researchers also profiled the relative abundance of major groups of fungi by depth in the soil profiles. They found that the upper soil layers are dominated by free-living saprotrophs (fungi that obtain their nutrition heterotrophically from non-living organic materials), and greater depths were dominated by mycorrhizal and other root-associated fungi. Their model suggests that these mycorrhizae live at the spots where the largest difference in carbon sequestration between the island size classes exists, which also tends to be the areas of highest root mass. When they ran tests for fungal biomass throughout each soil profile they found greater mycelial (the vegetative part of a fungus, consisting of a mass of branching, threadlike hyphae) production on large islands, but less mycelial necromass (dead stuff) on small islands. This suggests that the large production is counterbalanced by faster decomposition of mycelial remains. “Correspondingly, the 14C model indicated faster decomposition of root-derived [carbon] on large islands, despite inputs being conservatively constrained to be equal across all islands.”

I found these conclusions to be interesting because of the amount of soil carbon from roots and mycorrhizal fungi, especially on small islands. And although they saw less carbon accumulation on large islands, these islands have a greater root density and so should have more carbon allocation to roots and the associated fungi. Did you catch the contradiction? Well, in response to increased carbon dioxide, there will be an increase of carbon inputs to the roots which will accelerate the turnover of soil organic matter. This counteracts carbon accumulation and enhances nitrogen cycling through the microbial pools, an effect these researchers observed when they tested the C:N-ratios in the humus of large islands. This is much lower on small islands, possibly because of impared mycorrhizal nitrogen mobilization and the accumulation of nitrogen in fungal remains. This leads to progressive nutrient limitations, then leads to changes plant productivity, leading to changes in community composition, which leads to changes in total belowground carbon allocation, that leads to changes in fungi.

Definately starting to grasp the importance of the belowground dirty stuff. There’s a whole lot of carbon down there that we need to start looking at, accounting for, and seeing where it goes. We know that changes in the environment such as climate change, soil fertilization, fire suppression, and forest management make big differences to the aboveground stuff. It only makes sense that the belowground stuff is impacted as well.


Clemmensen, K., Bahr, A., Ovaskainen, O., Dahlberg, A., Ekblad, A., Wallander, H., Stenlid, J., Finlay, R., Wardle, D., & Lindahl, B. (2013). Roots and Associated Fungi Drive Long-Term Carbon Sequestration in Boreal Forest Science, 339 (6127), 1615-1618 DOI: 10.1126/science.1231923

If you would like some follow-up reading I suggest:

Treseder, K. K. (2013-03-29) Fungal Carbon Sequestration. Science, 339(6127), 1528-1529. (DOI: 10.1126/science.1236338) 

Also check out the write-up in Nature "Fungi and roots store a surprisingly large share of the world's carbon"

(image via Forest Keepers)

Castrating the Zombie Ant

Last year I posted Attack of the Zombie Ant! A post that turned out to be quite popular. To sum it up, there are fungal parasites (genus Ophiocordyceps) that infect ants and take control of their bodies. The fungus then compels the ant to crawl up into the forest canopy and clamp down on a leaf while the fungus grows inside the body, eventually producing a hyphae and stroma (fruiting body) that grows out of the head and produces and releases spores. And repeat.

A recent paper in PLoS ONE takes a closer look the coevolution between ant colonies and these rare, specialized fungi. Broadly, the term coevolution is used to describe how two or more species reciprocally affect each other's evolution. In the case of the zombie ants, it is host-parasite coevolution. The parasite evolves to infect the host, and the host evolves to resistant to the parasite. An arms race, if you will. The virulence and defense traits of specialized parasites, such as the zombie-ant fungi, are shaped by these arms races. This is even more true in species like Ophiocordyceps that rely on host behavior for their reproductive success. On the other side of the coevolutionary coin, ant colonies (in this case Formica and Camponotus ants) are long-lived and live in high density, continuously interacting colonies. This behavior has been shown to be a type of social immunity where there is a strong selection for efficient prophylactic defenses and where ant parasites pose a limited threat to infecting an entire colony. Meaning that individual ants my die from the fungal disease but that the mortality of the colony is low.

This paper specifically looks at the trade-offs experienced by Ophicordyceps manipulating ants into dying in nearby graveyards. When the fungus compels an ant to leave their nest and die close to their host colony, many infected individuals will end up in one area, forming high-density ant graveyards that may persist for years. Considering the life span of your average ant, that is a long time. The authors of this paper used data from previous studies of O. unilateralis in Thailand and collected a new data set from O. camponoti-rufipedis from Brazil to construct a developmental-stage-structured model describing this ant-fungus interaction. In this new collection, they identified ants infected with O. camponoti-rufipedis and marked areas covering entire graveyards, tagging all dead infected ants. Each cadaver ant was then characterized in terms of parasite development: (1) freshly killed ant, (2) dead ant with parasite stroma, (3) dead ant with mature fruiting body, (4) dead ant at stage 2 or 3, but hyperparasitized by other fungi, or (5) dead ant whose status could not be identified. To estimate the infectivity of the fungi's fruiting bodies, they collected a sample of dead ants and brought them to the lab for study. From these data, they were able to formalize the "life-cycle" of parasitized ants and calculate a growth rates and fungal developmental stage distributions of the graveyards.

The researchers found that only 6.5 percent of the O. camponoti-rufipedis fruiting bodies were effectively producing spores. Most of the dead ants that they found were sterile because they were either immature, damaged or hyperparasitized (secondarily parasite develops within a previously existing parasite). They also found that only 42 percent of the fruiting bodies were shooting spores at a particular time interval. When the apparently "healthy" cadaver ants were dissected, they found them to have been invaded by the larvae of small unidentified arthropods which may have reduced the likelihood of the fungi reaching maturity. Add to this that out of all of the ant colony members, only the foragers face the risk of encountering spores, then you end up seeing a rather low infection and transmission rate. So only if graveyards are stable or growing will infection levels be stable.

Interestingly, the authors found that the zombie-ant fungi are themselves vulnerable to attack by other parasites. Their model suggests that the stroma life stages or immature fruiting body stages are highly vulnerable to biotic attack. So much so that hyperparasitism is nearly negligible in the mature life stage. Whether that is because the mature life stage has a much more efficient immune defense or some other cause is unclear. What is clear is that hyperparasitic fungi prevent the infected zombie-ant fungus from spreading spores which, in turn, means that fewer of the ants will become zombies. This means that the rate of infections is much less than the size of some graveyards might suggest. It is known that O. unilateralis has a range of asexual stages (synanamorphs) with spores adapted for persistence or aerial dispersal. However, O. camponoti-rufipedis is known to produce a single anamorph. So the horizonatal transmission of this species may depend on the movement of the infected ants themselves. And that means all kinds of other intriguing studies may be in the works. Can't wait!


Sandra B. Andersen, Matthew Ferrari, Harry C. Evans, Simon L. Elliot, Jacobus J. Boomsma, & David P. Hughes (2012). Disease Dynamics in a Specialized Parasite of Ant Societies PLoS ONE, 7 (5) DOI: 10.1371/journal.pone.0036352


About the Authors:
Sandra Andersen's bio
David Hughes' Lab (includes zombie-ant videos on his Projects page)

Articles:
Penn State Science "The Zombie-Ant Fungus Is Under Attack, Research Reveals"
Discover Magazine "Zombie Ant Parasite Has Its Own Parasite - a Fungus that Attacks Fungi"
The Guardian "Zombie-ant parasitic fungus kept in check by hyperparasitic fungus"


(image from the Hughes Lab website)

The Human Biome

Wired recently posted an Atlas of the Human Ecosystem. It is a great infographic that includes some fantastic information. I'm posting their introduction, but follow the link at the end to see the full images.

"If some twisted genius vaporized all 10 trillion cells in your body — along with the hair, the fingernails, and other tissue they create — it would not leave empty space behind. A body-shaped cloud made of bacteria, viruses, and other former stowaways would hover briefly in the air. The cloud would outline your skin, delineate your lungs, trace your digestive tract. You might be gone for good, but your shadow biosphere would remain.

We got our first glimpse of these tiny tenants — now known collectively as the microbiome — in the late 17th century, when a Dutch lens grinder named Anton van Leeuwenhoek noticed a layer of white scum between his teeth. He mixed some of the gunk with pure rainwater and then placed it under one of his handmade microscopes. 'I found, to my great surprise,' he wrote, 'that it contained many small animalcules, the motions of which were very pleasing to behold.'

With the advent of fast DNA sequencing, today’s microbiologists can delve deep into this weird inner universe, and they’re just as amazed as Van Leeuwenhoek was. It’s not just the sheer quantity of microbial cells (100 trillion or so for one person alone) but also their diversity: Each of us is home to thousands of species of microbes, and no two people have quite the same mix.

We’re just beginning to learn the effects our microbiome has on us, but it’s clear that they can be profound. Certain species help digest food and synthesize vitamins; others guide the immune system. Medical researchers have linked obesity, heart disease, and anxiety to properties of the microbiome. In many cases, it’s not the individual species that seem to matter but the richness of the ecosystem. Just as the health of a forest depends upon diversity, our own health appears to benefit from the presence of a wide range of uninvited guests, many of which coevolved with us.

See below for a guided tour of your own personal ecosystem. From the top of your head to the depth of your gut, there’s a jungle in — and on — you."

Visit The Wired Atlas of the Human Ecosystem

Free Market Fungi

For today's post we are going to go below ground and get a little dirty. I read a great paper this week about symbiotic fungi that I really liked because it was a simple, elegant experiment that yielded neat results.

Let's start with defining mycorrhizae (mahy-kuh-rahy-zuh). These are specialized fungi that colonize plant roots, forming a symbiotic relationship, with over 90% of terrestrial plants having these fungi. The plant supplies the fungus with energy substrates, carbon (or sugars), for growth and development. The fungus supplies the plant with water and nutrients from the soil. It grows on the root but also extends an intricate network of hyphae through the soil, greatly increasing the surface absorbing area for the plant, sort of like having extended roots. They can also access hard-to-capture nutrients, such as organic nitrogen and phosphorus, and make them available for the plants to use. The benefits of having mycorrhizae are many. They allow for increased absorption efficiency, increased drought resistance, and increased pathogen resistance. It has also been shown that plants with mycorrhizae are overall healthier and less stressed, grow better as seedlings, and can be transplanted easier. And most plants have several different species of mycorrhizae on them at any one time.

There are three general types of mycorrhizae: (1) ectomycorrhizae, (2) endomycorrhizae, (3) orchid mycorrhizae. The distinction between the types is based on the morphology of the structure formed by the fungi and the plants, if there is penetration of the root cells or not. I'm going to leave out defining the orchid mycorrhizae because they are a pretty specialized group and just stick to the other two main ones. Ectomycorrhizas are mostly Ascomycetes and Basidiomycetes and are often found on woody plants. They are able to penetrate between, but not into, the cortical cells of the plants' root. Because of this, they form a thick hyphal mat that surrounds the root and a network of strands within the cortex called a "Hartig net." This type of fungus also forms a mantle which completely encloses the root tip, this is also where the hyphae extend into the soil. Endomycorrhizae or arbuscular mycorrhizas (alternately or formerly the vesicular-arbuscular mycorrhizas) are far more abundant and classified in the Order Glomales. Arbuscular mycorrhizas (AM) penetrate inside the walls of the cortical cells producing vesicles and highly branched structures called arbuscules.

A new paper in the journal Science takes a closer look at the symbiosis between plants and AM fungi. It is known that plants supply this fungi with carbohydrates and in exchange the AM fungi provide the plants with mineral nutrients (e.g., phosphorus) and the protections I listed above. However, the selective forces that maintain this mutualism are unknown. What keeps the plant from taking nutrients from the fungi and giving nothing back in return? After all, the plant is giving away nutrients that it would otherwise be using, incurring a cost. Or the fungi takes the carbon but gives nothing back to the plant? But if the symbiont interest are tightly aligned then the fungal symbionts should increase their own fitness by helping the plants, and vise versa. Makes sense, right? Now, add multiple fungal species, with each species simultaneously interacting with multiple plants. This is a great opportunity for "cheaters," fungi that exploit the benefits of getting food while avoiding the costs of supplying resources. This paper looks at the question of how these symbiotic partners maintain a fair, two-way transfer of resources. How they keep each other honest.

The researchers used the model plant Medicago truncatula (a small plant that looks kinda like clover) and three arbuscular mycorrhizal (AM) fungal species within the cosmopolitan subgenus Glomus Ab (Glomus intraradices, G. custos, and G. aggregatum). They chose these particular AM fungi because they are closely related and exhibited either high or low levels of cooperation (giving lots or little phosphorus). This cooperation was measured in plant growth responses, costs of carbon per unit phosphorus transferred, and resource hoarding strategies (fungal resource storage). They grew M. truncatula hosts with one, two (G. intraradices versus G. aggregatum), or all three AM fungal species. Then they followed the carbon flux from the plant to the fungi and the incorporation of host carbon into the RNA of the fungal assemblage (because it reflects C allocation patterns).

They found that more carbon was supplied to the more-cooperative fungal species. In both the two-species and three-species experiments the RNA of the cooperative fungus (G. intraradices) was significantly more carbon enriched than the less-cooperative fungus. In fact, the plants showed a host preference in communities where a more cooperative fungus species was available. The extent to which the mutualism can be enforced depends on the scale at which the plants can discriminate in this way. But because we are talking small little fungi, and lots of different kinds, the discrimination scale would need to be fine. This idea lead the researchers to the next part of their experiment, looking at whether fine-scale host discrimination occurs.

To test this they used an in vitro triple split-plate system. It sounds all complex but is actually rather simple. They took a petri dish and divided it into 3 equal sections or compartments.One compartment had mycorrhizal roots and two have fungi composed of the same fungal species but varying in phosphorus supply. Its a good system because it allows the root to "choose" which fungus it wants to partner with based on the amount of nutrients (carbon) transferred from the fungus. They also tested the reverse - if the fungi enforced cooperation by the plant. They used the same split-plate system but used one fungal compartment and two root compartments, making the fungi choose which root it wanted to partner with.

The researchers found that the plant rewarded the fungus that supplied the most phosphorus, more carbon was transferred to the fungus with access to more phosphorus. In the reverse test they found that the cooperative fungus (G. intraradices) transferred more phosphorus to the roots with greater access to carbon resources. So both the plant and the fungi are discriminating. In the less-cooperative species (G. aggregatum) no carbon allocation differences were found, and it transferred more phosphorus to the roots with more carbon access but stored the phosphorus in a host-inaccessible form. It was a little phosphorus hoarder, tsk tsk.

And finally, the researchers wanted to determine whether the fungi are stimulated to provide more phosphorus in direct response to a greater host carbon supply. So they created an experiment to track the simultaneous resource exchange between the plant and fungi by using a two compartment plate and exposing the roots to labeled carbon (U-¹⁴C sucrose) in either high or low concentrations and adding labeled phosphorus (³²P) to the fungal compartment. They found that increasing the carbon supply stimulated the phosphorus transfer by the cooperative fungus but not the less cooperative fungus.

Overall, this paper shows that the mutualism in this system is different than that you find other systems. It isn't controlled by only one partner but, instead, both sides interact with each other to keep the other honest. Each of the partners cooperates with the other, preferentially rewarding them for good service. And this is where the title for this post comes from. The authors equate this system to a market economy, "where there are competitive partners on both sides of the interaction and higher quality services are remunerated in both directions."

Kumbaya.

Read the entire paper here:
Kiers, E. Toby, et al. (2011) Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science: 333(6044), 880-882. (DOI: 10.1126/science.1208473)

Learn more about mycorrhizae here:
The Davies Lab at Texas A&M University
Botany at the University of Hawaii
Foresty 442 Notes from Oregon State University

(image from dirtdoctor.com)

Batting a Billion

Did you know that 2011-2012 is the Year of the Bat? Thanks to classic literature and popular culture, bats are thought to be nocturnal, creepy, winged rats. Probably every fear people have concerning bats is based on centuries of myths and misinformation. As part of my what-is-becoming-typical subject introduction I thought I'd give some facts and dispell a few of the myths about bats with a little round of True or False. As I plan to present a paper here and not just a bunch of bat facts I'll try to keep to some of the most popular myths and at the end of this post I'll have some links where you can find out more information.

True or False?: Bats are mammals.

TRUE

Bats are flying mammals belonging to the order Chiroptera. There are more than 1,100 species (that's 1/5 of all mammals!), including the world's smallest mammal, a bat the size of a bumblebee.

True or False?: Bats are blind.

FALSE

Actually many bats have very good eyesight. However, because many species are nocturnal (active at night) they have an extra sense that helps them to navigate and find food: echolocation. They send out sound which bounces back off of objects and creates a sort of map for the bat.

True or False?: All bats feed on blood.

FALSE

Well, mostly. Admittedly there are three species of vampire bat: the Common Vampire Bat (Desmodus rotundus), the Hairy-legged Vampire Bat (Diphylla ecaudata), and the White-winged Vampire Bat (Diaemus youngi); all of which are found in Latin America. But don't worry, they don't require much blood and typically like to feed on livestock. More than two-thirds of bat species are primary predators of night-flying insects, this includes agricultural pests and many insects humans find to be particularly disruptive or annoying. A single bat can eat up to 1,000 mosquito-sized insects in a single hour! The other third of bat species feed on the fruit and nectar of plants. As such, they serve as pollinators and seed dispersers for many plant species. A small percentage are also known to eat fish, frogs, mice, birds and/or other small vertebrates.

True or False?: Bats are found everywhere.

FALSE

Close but no. Bats are a very diverse group that take advantage of a wide variety of habitats, but they do not inhabit extreme desert and polar regions.

True or False?: Bats live in caves.

TRUE

You can find many bat species living in caves. This is because one of the most basic requirements for bat is a safe roost. As such, bats can be found living in almost any conceivable shelter, from caves to buildings to leaf cavities and even in animal burrows. As their habitats shrink, more and more species, and individuals, can be found living in buildings. Building bat houses, the same concept as a bird house, is a backyard conservation technique that is catching on with the public. (Learn how to build you own bat house here: http://www.batcon.org/index.php/get-involved/install-a-bat-house.html)

The questions that I've listed here are not only some of the most popular concerning bats, they are also directly related to today's topic. A new Policy Forum paper published in Science this week takes a look at bat conservation from the aspect of their economic importance.

It is known that White-nose Syndrome (WNS) and the increased development of wind-power facilities are threatening populations of bats in North America. WNS is a fungus (Geomyces destructans) that infects the skin of cave-dwelling bats while they hibernate, particularly around the nose, ears, and wings. It is associated with a high mortality rate and is estimated to have killed over a million hibernating bats in more than 15 U.S. states and 2 Canadian provinces. Little Brown Bats (Myotis lucifugus) are sustaining the highest mortality rates, showing a 93% decline in 23 caves at the epicenter of the WNS outbreak. Other species affected include the Big Brown Bat (Eptesicus fuscus), Northern Myotis (Myotis septentrionalis), Tri-Colored Bat (or the Eastern Pippistrelle, Pipistrellus subflavus), Eastern Small-Footed Myotis (Myotis leibii), and Indiana Bat (Myotis sodalis).

Our growing concerns about climate change mixed with our desire to break our dependance on oil have resulted in the construction of more wind turbines. As a source of alternative energy wind turbines are a wonderful thing. However, for species of migratory tree-dwelling bats they are a flight, and life, hazard. In North America, these species include the Eastern Red Bat (Lasiurus borealis), the Hoary Bat (Lasiurus cinereus), and the Silver-haired Bat (Lasionycteris noctivagans). Other species that are ssusceptible to wind turbines include the Tri-colored Bat (L. subflavus), the Little Brown Myotis (M. lucifugus), and the Big Brown Bat (E. fuscus), species names that should sound familiar after reading about WNS. Included in this list of affected species includes bats with a relatively small range sizes, the Mexican Free-tailed Bat (Tadarida brasiliensis) and the federally endangered Indiana Myotis (M. sodalis). High numbers fatalities in species with small range sizes has a greater impact on the survivability of the species than the same number of fatalities in populous, large-range species. It is still unclear why these species are so susceptible to wind turbines. There is no continental-scale monitoring programs for assessing wildlife fatalities caused by wind turbines, but it is predicted that by 2020 an estimated 33,000 to 111,000 bats will be killed by wind turbines just in the Mid-Atlantic Highlands of the U.S.

This article focuses on these two sources for declining bat populations, leaving out sources such as habitat degradation. The numbers of bat fatalities are, in and of themselves, pretty staggering, but many people in political and policy making positions still consider it an academic interest rather than an economic problem. That is where this article becomes particularly interesting. In fact, the economic consequences of losing so many bats could be substantial. One example the authors use is the Big Brown Bat (E. fuscus). A single colony of 150 bats in Indiana as been estimated to eat nearly 1.3 million pest insects per year. Think about it: That is one relatively small colony of bats eating a whole lot of insects. Other estimates have a single Little Brown Myotis (M. lucifugus) consuming 4 to 8 grams of insects each night. Doesn't sound like much, but if you extrapolate that from one bat to one million bats that is 660 to 1320 metric tons of insects. This is a huge disruption to the population cycles of agricultural pests, and to say that bats are unimportant is just ignorant. 

The paper goes on to discuss the economic importance of bats in agricultural systems, estimating the value of the pest suppression services provided by bats. Previously published estimates have the value at anywhere from $12 to $173 per acre, with a likely value at $74/acre in a cotton-dominated landscape in south-central Texas. The authors here took these values and extrapolated the estimates to the entire United States. They estimated that the value of bats to the agricultural industry at between $3.7 billion and $53 billion per year with a likely value of approximately $22.9 billion per year. This cost does not include any downstream impacts of bat loss such as the impact of pesticides, secondary predation, and the predator release of insect populations.

A figure describing the worth of bats. Yellow being low cost to red being high cost.

 In terms of policy, the authors suggest that wait-and-see approach to the issue of widespread declines of bat population is unacceptable as the life histories of these mammals suggest that population recovery is unlikely for decades or centuries, if at all. They suggest management actions to restrict the anthropogenic spread of WNS, taking additional steps toward developing improved diagnostics to detect early stage infections and fungal distribution, investigating biological or chemical control of the fungus, increasing disease resistance through habitat modification, potentially culling infected bats, altering wind turbine operations during high-risk periods for bats, and continued research into these problems.


Here's the article:
Justin G. Boyles, Cryan Paul M., McCracken Gary F., and Kunz, Thomas H. (2011) Economic Importance of Bats in Agriculture. Science: 332 (6025), 41. (DOI: 10.1126/science.1201366)

GENERAL INFORMATION ABOUT BATS:
Description of bat species from the Smithsonian National Museum of Natural History:
http://www.mnh.si.edu/mna/image_menu.cfm?order=4
Info on bats from the Natural Science Research Laboratory at the Museum of Texas Tech University: http://www.nsrl.ttu.edu/tmot1/ordchiro.htm
The Year of the Bat website:
http://www.yearofthebat.org/
From Boston University's Bat Lab: http://www.bu.edu/cecb/bats/bat-facts-and-folklore/
From the Museum of Palentology at UC Berkeley:
http://www.ucmp.berkeley.edu/mammal/eutheria/chiroptera.html
A list of academic "bat labs": http://www.science.mcmaster.ca/psychology/faurelab/links

BATS AND WIND ENERGY:
From Bat Conservation International:
http://www.batcon.org/index.php/what-we-do/bats-and-wind-energy.html?utm_source=internal&utm_medium=five_icon&utm_campaign=5IBats%2B%26%2BWind%2BEnergy
Bats and Wind Energy Cooperative (BWEC): http://www.batsandwind.org/
Video and information from Boston University about bats interacting with wind turbines:
http://www.bu.edu/cecb/wind/video/
U.S. Department of Interior, US Fish and Wildlife Wind Turbine Guidelines Advisory Committee:
http://www.fws.gov/habitatconservation/windpower/

WHITE-NOSE SYNDROME (WNS):
Buzbee's Bathouse Page:  http://www.batbox.org/
Info from the U.S. Fish and Wildlife Service: http://www.fws.gov/WhiteNoseSyndrome/
From the Organization for Bat Conservation:
http://www.batconservation.org/drupal/white-nose?gclid=CKy6l6rO-6cCFUNl7Aod6R0srw
USGS National Wildlife Health Center WNS Page:
http://www.nwhc.usgs.gov/disease_information/white-nose_syndrome/
The National Speleological Society's WNS Page:
http://www.caves.org/WNS/

BAT CONSERVATION ORGANIZATIONS:
Bat Conservation International: http://www.batcon.org/
Organization for Bat Conservation: http://www.batconservation.org/
Bat Conservation and Management, Inc.: http://www.batmanagement.com/main.html
Lubee Bat Conservancy: http://www.batconservancy.org/
Bat World Sanctuary: https://batworld.org/
Bat Conservation Trust (in the UK): http://www.bats.org.uk/
The Warwickshire Bat Group (UK):  http://www.warksbats.co.uk/
The Norfolk Bat Group (UK): http://www.norfolk-bat-group.org.uk/index.html

(image from discoverlife.org)

Attack of the Zombie Ant!

A couple of years ago a study was published in The American Naturalist about an interesting fungal parasite known as Ophiocordyceps unilateralis. This fungus infects ants in the tribe Camponotini (carpenter ants) but does not kill them outright. Rather, the ant remains alive for a short time but the fungus is in control. The fungus compels the ant to crawl down from its nest in the high forest canopy down to the small plants of the understory. Then the fungus has the ant crawl onto the underside of a leaf, clamp down its mandibles, and then die. There the ant body will stay while the fungus continues to grow inside of its body, producing a hyphae and stroma (fruiting body) that grows right out of the ant's head. The stroma then releases spores on to the forest floor, spores waiting to infect the next unsuspecting ant passerby. You can see where the nickname "zombie ants" and "zombie fungus" came from. Now, this was not a previously unknown species of fungus but rather an unknown effect of the fungus on ants, a previously unknown part of the life cycle. What is truly amazing is the accuracy to which the fungus directed the ant. The ants always clamped on to the underside of a leaf and almost always on a leaf vein. The chosen leaf was about 25 centimeters above the ground, with 94-95% humidity, and between 20-30 Celsius. The fungus directs the ant to a location with the parameters that it needs to survive and reproduce.

Now a new paper in the journal PLoS ONE describes four new species belonging to the O. unilateralis species complex from the Atlantic rainforest in Brazil. The species are named according to their ant host species (specifically Camponotus rufies, C. balzani, C. melanoticus, and C. novograndadensis). Ultimately, this paper is just recognizing and naming new species. However, it helps to draw attention to the south-eastern region (Zona de Mata) of the State of Minas Gerais in Brazil, one of the most heavily degraded biodiversity hotspot on the planet. A total of 92% of this rainforest is gone, and four new species have just been discovered. How many more are there to find and how many have already been lost?

Want more zombie animals? Check out these:
The nematode-ant relationship in Central America
The emerald cockroach wasp (Ampulex compressa)-cockroach relationship in the Polynesian Islands.
The spider (Plesiometa argyra)-wasp (Hymenoepimecis argyraphaga) relationship in Costa Rica.

The list goes on and on; pill bugs and spiny-headed worms (Plagiorhychun cylin-draceus), grasshoppers (Melanoplus sanguinipes) and the protist (Nosema acridophagus), the fluke (Dicrocoelium dendriticum) and the ant, the wasp (Glyptapanteles) and the caterpillar, the distome (Leucochloridium paradoxum) and the snail, the barnacle (Sacculina carcini) and the crab, etc. Wasps, ants, and caterpillars tend to have a lot of parasite-host stuff going on (there's even a whole group of parasitoid wasps), although admittedly not all that much zombism. It is an ever-so-interesting evolutionary arms race!

Read more about zombie animals here: http://www.newscientist.com/article/mg14018983.500-evolutions-neglected-superstars-there-is-nothing-glamorous-about-fleas-flukes-or-intestinal-worms-so-why-are-they-suddenly-attracting-so-much-attention.html
and here: http://discovermagazine.com/photos/04-zombie-animals-and-the-parasites-that-control-them

The original zombie ant study (online version of the paper contains a video):
Andersen, Sandra B., et al. (2009) The Life of a Dead Ant: The Expression of an Adaptive Extended Phenotype. The American Naturalist: 174(3), 424-433. (DOI: 10.1086/603640)

The new study, and because it is published in PLoS ONE it is free access (yay!):
Evans, Harry C., Simon L. Elliot, and David P. Hughes. (2011) Hidden Diversity Behind the Zombie-Ant Fungus Ophiocordyceps unilateralis: Four New Species Described from Carpenter Ants in Minas Gerais, Brazil. PLoS ONE: 6(3), e17024. (DOI:10.1371/journal.pone.0017024)

Online stories on this paper:
http://blogs.plos.org/everyone/2011/03/02/four-new-species-of-zombie-ant-fungi-another-step-forward-for-open-access-taxonomy/%20
http://www.physorg.com/news/2011-03-species-zombie-ant-fungi-brazilian.html
http://www.sciencedaily.com/releases/2011/03/110302171309.htm

Fungi Phylum Fun

I love great, musical biology projects. Fungi!

Hot and Spicy

When you think of fruit what do you envision? A sweet, juicy treat? That's what I think of, particularly strawberries. Mmmmmm....

This sweet, juicy goodness, evolutionarily speaking, is a reward to animals for the dispersal of the fruits' seeds. In fact, it is considered to be one of the key innovations in the radiation of angiosperms (flowering plants). However, the plants don't receive just the goodly seed-dispersers, they also end up attracting consumers (vertebrates, invertebrates and microbes) that are detrimental to the plants' fitness (put very very simply, how much it reproduces). These detrimental consumers come in the form of seed predators that reduce the likelihood of seed dispersal and viability. The middle ground or balancing factor comes in the form of the fruits' chemistry. The makeup of the fruit can deter seed predators, reduce microbial attack, and/or attract specific seed dispersers, all without compromising seed viability. Generally, this explains the presence of noxious, bitter, and sometimes toxic chemicals in many ripe fruits.

Now that we know some general fruit stuff, how do we test something like the variance in microbial pathogen pressure as it is related to the variance in the chemistry of wild, ripe fruits? Well, you would need to start with a fruit species in which you know the chemistry pretty well. You would then need to show that the chemistry of the fruit deters microbial pathogens. Start playing with concentrations of both and you've got yourself an experiment.

Hmmm...what is a fruit that deters things from eating it? If you've looked at the picture above then you can probably guess: Chilies. Chilies belong to the genus Capsicum and were one of the first plants to be domesticated in the New World. They contain what are called capsaicinoids, which produce the spicy/hot capsicum (hotter = more pungent fruit), are unique to this genus, are well characterized, and are broadly antimicrobial. Capsaicinoids also increase in their concentrations during fruit ripening and are limited to the fruit itself (rather than to other parts of the plant). The authors of this paper also rediscovered a polymorphism for capsaicinoid production in wild populations of multiple chili species which allowed them to test the variability of these chemicals in the wild.

The researchers did most of their work with Capsicum chacoense Hunz., which is native to the Chaco region of Bolivia, Argentina, and Paraguay. They used a geographic gradient to study the impact of microbial pathogens on fruit chemistry. The results showed that across all populations the only significant cause of fruit and seed damage was microbial infection, primarily caused by the fungus Fusarium semitectum. This particular fungus enters the fruit by way of the piercing proboscises of hemipteran bugs. On closer inspection they found that the fungal infection of seeds increased with the number of foraging scars on the fruit and that fruits with no insect damage had no fungal infection. This pattern was seen in both pungent and nonpungent fruits, but the slope of the relationship was significantly steeper for nonpungent fruits, the infection rates for nonpungent fruits being almost twice as high. Because pungent and nonpungent fruits are indistinguishable in the wild there must be something else going on. When the scientists created an artificial fruit media that mimicked the nutritional composition of the C. chacoense fruit except for the presence/absense and concentration of capsaicinoid chemicals they found that the inhibition of F. semitectum was dose-dependent. The reduction of infection by F. semitectum was completely accounted for by the capsaicinoid chemicals.

The protection that chilies receive from these chemicals shapes the chemistry of the fruits, provides a selection pressure to the fungus, and explains among-population variation of capsaicinoid production. As fungal pressure increases there will be an increase pungent phenotypes in the chilies. So why not just stay hot and spicy all the time? As with most things there is a trade-off. If the plant puts more into chemical production it puts less into seed coats. That means that pungent plants will protect their seeds from fungal infection but those seeds will not be as well protected when they travel through the digestive system of a seed disperser. You get the idea right?

Being firmly in the medium-salsa crowd I must then ask, why do humans love the hot stuff? Some argue that chilies help lower blood pressure, that the antimicrobial effects also benefit us, and that they increase salivation allowing for better digestion. All good notions, in my opinion, but that's still not gonna make me eat a super-hot chili. No way. According to a NY Times article on this topic, Dr. Rozin (who studies human emotions, likes, and dislikes) says he has evidence for what he calls benign masochism. In the article, Dr. Rozin says that in his experiment he tested chili eaters by gradually increasing the pungency of the chili until they said they could go no further. He then asked what level of heat they liked the best, and they chose the highest level of unbearable pain. Crazy? I think so. I'll stick with bell peppers, thank you.

Here is the paper on chili evolution:
Tewksbury, Joshua J., et al. (2008) Evolutionary ecology of pungency in wild chilies. PNAS: 105(33), 11808-11811. (DOI: 10.1073/pnas.0802691105)

And this is the NY Times article:
http://www.nytimes.com/2010/09/21/science/21peppers.html

(image from topnews.in)

Cellulotastic

A colony of the fungus Neurospora crassa (left) growing on cellulose and the yeast Saccharomyces cerevisiae. Sugar transporters from Neurospora that have been inserted into the yeast are tagged with green fluorescent protein. (Image: Jamie Cate and Susan Jenkins, UC Berkeley & EBI)

Reseachers at the University of California, Berkeley have been working on how and what yeast can digest. They have taken genes from a grass-eating fungi (Neurospora crassa) and put them into yeast. This new set of genes allows the yeast to produce alcohol from cellulose, a material that is normally indigestible. N. crassa is one of the rare yeasts that can digest cellulose because its preferred diet is fire-damaged plants. The genes were located by doing a genome-wide systems analysis to see which genes are turned on when the fungus grows on cellulose. The researchers were able to locate a family of genes which produces proteins that transport sugars into the Neurospora cell to be used a fuel and some transporters, in particular, that allow the cell to import a few types of cellodextrins (specifically cellobiose, cellotriose, and cellotetraose), simple-ish sugars.

Why should we care what yeast are able to digest? The biofuels industry has been struggling to make cellulosic ethanol economically feasible. Right now the industry is using brewers yeast, the single-celled fungus (Saccharomyces cerevisiae) to turn sugar or other simple carbohydrates into alcohol. So far cellulose has been a bit of a problem as it is a pretty tough molecule; it is composed of glucose (simple sugar) molecules all linked together into long chains. Its a molecule that you can find in abundance in various materials such as corn stalks, leaves and cobs (and the US uses a whole lotta corn!) as well as paper waste or any other plant material. Normally these long chains have to be broken up into smaller cellodextrins by enzymes called cellulases using a method called saccharification. Then another enzyme called beta-glucosidase is added to break down the cellodextrins into their simple sugar components. That's all before the yeast even get introduced to the system! If the N. crassa genes (cellodextrin transporters) can be inserted into the industrial strains of yeast that are currently being used for ethanol production the efficiency of the fermentation process can be greatly improved.

The paper appeared in this weeks ScienceExpress:
Galazka, Jonathan M., et al. (2010) Cellodextrin transport in yeast for improved biofuel production. Science: published online. (DOI: 10.1126/science.1192838)

Here is UC Berkeley's new article about the paper:
http://berkeley.edu/news/media/releases/2010/09/09_neurospora.shtml