A forest on glass beads

Defying all expectations,  a forest has grown on the beach. Just east of Philadelphia is  the New Jersey Pine Barrens- a vast wilderness almost completely ignored outside of a small group of park rangers, volunteer fire fighters and hardy locals whose families have eked out a subsistence living here for generations. And yet is is considered the largest undisturbed wilderness in the northeastern corridor with a incredibly unique ecology and a set of rare endemic species.

The Pine Barrens region spans most of southeastern New Jersey from the Atlantic coast inland across the mid-Atlantic coastal Plain. The coastal plain is essentially a huge wedge of sand that has accumulated over 5 million years of sedimentary deposition from the Applalachian mountains and southerly flowing rivers such as the Hudson. A long history of sedimentary accumulation has created a flat, unvarying topography. 18 feet of height divide the highest point in the Pine Barrens “uplands” region and the lowest point in the “lowlands”, and yet this seemingly homogeneous landscape has produced broad environmental gradients over incredibly short distances.

The reason for these gradients seems to relate to the unique nature of the sandy, nutrient depauperate soil. Sand can act as either a sieve or a water trap depending on its spatial position. At higher elevations,  rain drains freely through the sandy soils, leaching away any nutrients that accumulate and producing highly acid conditions that few plants can survive on. The uplands forests are dominated by drought-resistant, fire-tolerant pitch pine trees with a smattering of oaks. A few scrubby, low-nutrient requiring members of the Ericaceae family, such as huckleberry and highbush blueberry, dominate the understory. At low elevations, rain accumulates and has nowhere to go. The water table is generally high, producing soils that are saturated year-round. In the most saturated places, one finds peat bogs and white cedar swamps more reminiscent of the deep south than the mid-Atlantic. Swamps grade into tall, shady oak-dominated forests dotted with an occasional pine in the drier lowlands.

The stark contrast between uplands and lowlands vegetation is not just a product of  the soil conditions. The uplands and lowlands communities produce feedbacks on the environment that maintain the land in precisely the same condition for generations, such that nothing new can manage to gain a competitive edge.

In the uplands,  pine trees exude organic acids into the soils, maintaining their soils in a state of poor nutrient quality that nothing else can survive on. Every few years pines drop their needles, but not before sucking nearly all the nutrients out and back into the branches, ensuring that few nutrients are added back to the soil. The low nutrient-quality of this leaf litter slows microbial decomposition, causing years of litter to accumulate on the surface. This litter serves as kindle that enhances the spread of forest fires the pine trees require to sprout. These forest fires keep the less fire-resistant oaks at bay.

In the lowlands, wet conditions prevent forest fires from scorching the landscape with regular ferocity seen in the uplands. Oak trees are able to gain a firmer footing here, and once established, produce a shady understory that pine saplings cannot survive in. The oak trees drop their leaves annually, adding more nutrients to the ground and producing a soil richer in organic matter than enhances the development of a herbaceous understory, which helps crowd out pine saplings.

I stood over a pit we had just dug in the ground, staring down into what resembled a layer cake of dark chocolate, vanilla and red velvet. Distinct stratification in the soil profile  generally indicates a long history of mobilization processes. Organic matter leached down through the chocolately topsoil will sometimes produce a white, organic-free layer beneath, known to soil scientists as an E-horizon. Deeper still, weathering products from the underlying bedrock will accumulate in the subsoil and form complexes with the organic matter that has been transported down. The reddish layer I was seeing in the deep soil was the result of iron accumulation and subsequent oxidization by microbes in need of an energy source. In fact, the entire soil profile, from brown to white to red, is very typical of a class of soils known as Spodosols that dominate the New England and Canadian boreal forests, where low temperatures cause decomposition and other soil-forming processes to occur slowly, resulting in a surface buildup of organic matter and eventually the formation of distinct, colorful stratified layers. What, then, was such a soil doing in the Pine Barrens, a much warmer climate than New England, and a region with few soil nutrients and barely any organic matter inputs?

It turns out that the Pine Barrens soils which so closely resemble Spodosols may in fact be a relic from a much earlier time and different climate. At the height of the Last Glacial Maximum approximately 18,000 years ago, a large continental ice sheet known as the Wisconsan Glacier ended a mere 40 miles north of the Pine Barrens.  The New Jersey climate probably resembled those seen in the high Canadian boreal today, and there is little doubt that the soils that formed were some version of Spodosols. It is entirely possible that, given the state of extreme stasis that the Pine Barrens have existed in since the beginning of the Holocene, not much has occurred to alter the soils from their former state.  A forest that grows today on glass beads has thrived because of its ability to maintain stasis. Peeling back the layers of that forest reveals this stasis to be true, but only for a fleeting moment in the geologic record.

The microbial loop theory: 30 years of cross-Atlantic communication barriers

The more forest ecologists learn about plant nutrients, the more evidence accumulates that plants are not simply passive organisms whose chances of survival are based on environmental factors outside of their control.  In acquiring basic nutrients from the soil, one may well imagine that a plant’s success is dependent on chemical properties of the soil alone. By simple “luck of the draw”, plants that seed in nutrient-rich spots will grow faster and larger than plants seeding in nutrient poor regions.

In several of my previous posts, I’ve addressed this issue one way or another, talking about plant-mychorrizhal associations and root-grafting as strategies that allow less fortunately placed plants to acquire sufficient nutrients to survive. I’d like to now address an entirely different theory concerning plant nutrient acquisition, one which, despite thirty years of European research, remains hotly contested and represents one of the major theoretical divides between European and American soil/plant ecologists.

The microbial-loop theory is a paradigm developed several decades ago and has become a cornerstone of European thinking about how plants interact with other soil organisms. In essence a relatively simple idea, the microbial loop would, if proved, require the reevaluation of a huge body of North American literature about plant nutrient acquisition, which generally argues that that basic nutrient demands and stoichiometric constraints- most notably nitrogen limitation in temperate forests and phosphorous limitation in the tropics, exert a fundamental control over forest productivity.

It is well known that plants exert significant control over the processes that occur in the rhizosphere, a narrow zone of soil and pore space that surrounds their roots. Here, plants dump simple sugars such as glucose in order to nourish an active microbial community. They apparently do so because microbes exhibit a diverse array of metabolic capabilities that plants themselves do not have. Microbial processes release essential nutrients, such as nitrogen, from complex organic matter in a plant-soluble form. This much about plant-microbe symbioses- trading carbon for nitrogen or another plant-limiting nutrient- is agreed upon by American and European scientists.

We start entering hot water when we look more closely at the actual microbial players in this game- who are they and what exactly are they doing? “Microbe” is really a very generic term that can refer to pretty much any organism that is invisible to the unaided eye. Within this umbrella grouping, two slightly more specific classess of organisms seem to be important in the rhizosphere: protozoa and bacteria. Bacteria are the tiny prokaryotic organisms that are largely responsible for decomposition and the release of plant-available nutrients. Protozoa, however, are single celled eukaryotes. They are larger, have more complex cellular organization, and importantly, feed on their smaller bacterial neighbors. Any soil sample that contains bacteria almost certainly contains protozoa as well. The relationship between these two groups of microorganisms represents a classic and well-studied predatory-prey model.

So, given that plants are feeding microbes by dumping sugar into the soil, who is the sugar intended for? The bacteria, or the protozoa? The classic paradigm would argue that the bacteria, as the important nutrient-acquiring organisms, are the intended recipients of plant carbon exudates.

But what does this make the protozoa? Are they just thieves, stealing a farmer’s corn that was intended to feed his cattle? Numerous studies have shown that protozoan populations increase dramatically in the presence of plant carbon exudates because they are using the carbon themselves. A high-energy, readily available food source is just as appealing to protozoa as it is to bacteria.  Why would plants, that have perfected so many survival strategies over evolutionary time, allow this to happen?

The microbial loop theory argues that it is the protozoa that plants are “cultivating”. Why? Protozoa prey on bacteria, and bacteria, remember, are full of the nutrients that plants need. After eating a bacteria filled meal, a protozoa will likely excrete those same nutrients, making them available for plants. The protozoa are a conduit, passing nutrients to plants that would otherwise be locked up in the bacterial community.

There is mounting evidence from various lines of research in support of the microbial loop theory. Experiments have shown that early in development, plant root architecture is dramatically altered in the presence of protozoa. Increased root branching increases surface area, or “real estate” that protozoa can inhabit. “Tracer” studies, using a labeled isotope of a nutrient, are now providing evidence for a flow of soil nutrients from bacteria to protozoa before becoming plant-available. Finally, molecular studies of bacterial communities reveal an increased abundance of less-palatable bacterial species in the presence of protozoa, and an increased frequency of genes involved with bacterial defense. This genetic evidence underscores the importance of protozoan predation in structuring bacterial communities. Soon, perhaps, nano-cameras will be available to visualize what is actually happening in the rhizosphere between plants, bacteria and protozoa.

The importance of understanding this interaction is not trivial.  The means by which plants get their nutrients has ramifications for ecosystem productivity, ecosystem nutrient cycling, and responses to environmental change. Should we progress forward in the field of ecosystem science, a critical reexamination (and open discussion!) of what exactly is going on in the rhizosphere between plants and they critters they cultivate is necessary.

A detailed review of microbial loop theory and a paper that addresses some of the important counter-arguments:

1.    Bonkowski, M. Protozoa and plant growth: the microbial loop in soil revisited. NEW PHYTOLOGIST 162, 617-631 (2004).
2.    Ekelund, F., Saj, S., Vestergard, M., Bertaux, J. & Mikola, J. The “soil microbial loop” is not always needed to explain protozoan stimulation of plants. SOIL BIOLOGY & BIOCHEMISTRY 41, 2336-2342 (2009).

Earthworms play key role in regulating carbon storage in tropical ecosystems

A principle frontier in our understanding of global carbon budgets is tropical forests, on which research is historically scarce. At temperate and high latitudes, a warmer climate is predicted to increase the rate of decomposition and soil carbon turnover, resulting in a positive feedback on atmospheric carbon as CO2 is released from soils at increasing rates. A better understanding of the mechanisms regulating tropical carbon storage is needed in order to develop a holistic picture of global carbon cycling and feedbacks due to climate change.

Earthworms are important regulators of many ecological properties of soils. Their burrowing activity increases soil pore space and contributes to soil structure and drainage. Most importantly, earthworms can digest a huge quantity of dead and partially decomposed plant material. This digestion causes chemical transformations that ultimately produce nutrient-rich soil organic matter, or SOM. SOM helps ensure soil fertility, and contributes to numerous physical and chemical soil properties such as soil structure, porosity, water retention, and the capacity of soils to buffer pH changes. SOM’s aggregate structure causes it to have high water stability. This is an essential property in tropical forests, which have the highest rainfall levels of any biome on Earth.

SOM produced by earthworms is also rich in both carbon and nitrogen. A detailed biochemical and molecular analysis of earthworm casts suggests that these creatures may in fact play a key role in controlling tropical carbon storage.

Casts are clumps of digested organic matter excreted by earthworms that aggregate into large and distinctive structures. Researchers working in the rain forest neighboring the Dong Cao village in Northeast Vietnam studied the effect of cast production by Amynthas Khami on soil C storge. A. Khami is a species of tropical earthworm that can grow up to 50 cm long and produce tower-like casts. The researchers first used a “simulated rainfall” experiment to determine the relative stability of casts versus control soils. They then measured total carbon content, lignin and mineral-bound SOM content of casts and control soils.

An earthworm cast produced by A. Khami, a large tropical species found in Northeast Vietnam.

The study found striking differences in the chemical composition of earthworm casts versus control soils that ubiquitously indicate higher carbon storage in casts. Casts are more structurally stable and can withstand at least twice as long a rainfall event as control soils without compromising their structural integrity. They are enriched in carbon compared with controls, and particularly in carbon compounds such as lignin that have a high “carbon storage” potential. Lignin, a primary constituent of woody plant tissue, is a complex and heterogeneous molecule that is both carbon-rich and difficult for microbes to decompose. Earthworms probably excrete high quantities of lignin after obtaining the more digestible carbon sources from the roots and leaves that they eat. Finally, high levels of mineral associated-SOM were found in casts. Soil minerals bind to organic matter through electrostatic interactions, and in doing so make it unavailable for decomposers.

Though it well known that earthworm digestion initially speeds up decomposition, this new study suggests that casts may in fact contribute to long-term carbon stabilization. In tropical soils, which tend to cycle carbon quite rapidly, this mechanism should not go unappreciated. Future tropical land-use decisions may want to account for the welfare of this often-unappreciated soil organism.

Hong et al. 2011. How do earthworms influence organic matter quantity and quality in tropical soils? Soil Biology and Biochemistry 43: 223-230.