It’s all happening at the ecotone

In an effort to make order out of the chaos of existence, scientists often resort to classifying stuff.  To make order of the natural world, ecologists classify different regions of the world into distinct biomes – large geographical areas with characteristic groups of organisms adapted to that particular environment.  Familiar examples of terrestrial biomes are tropical forests, temperate grasslands and desert, and in the aquatic world examples include open ocean, coral reefs and rivers. But what happens at ecotones, where two or more biomes come together? Research has shown that ecotones can be biodiversity hotspots, as the diverse habitats attract many different species, and may also attract edge specialists – species that are particularly adapted to conditions on the border between the two biomes.


Sara Weinstein collects data at the ocean to land ecotone. Credit: Anand Varma.

Sara Weinstein’s graduate research explored the ecology and transmission of raccoon roundworm, Baylisascaris procyonis, a widespread raccoon parasite that causes severe disease in other animals (including humans).  She was dissecting raccoons to study infection patterns and as she describes “it would have been a waste of perfectly good raccoon guts to not also examine the rest of the parasite community.”  This examination would allow her to determine whether the generalization that ecotones are biodiversity hotspots for terrestrial and aquatic organisms also applies to the much more murky world of gut parasites.


A raccoon poses next to a culvert. Credit: SB Weinstein.

Working with four other researchers, Weinstein compiled a database of published accounts of gastrointestinal parasites from surveys of 256 raccoon populations.  They then used this database to classify parasites as either core or satellite.  Core parasites are locally abundant, common over a large region and can occupy a broad ecological niche.  Satellite parasites are rare, restricted to a small portion of a region and have narrow ecological niches.


Microphallus sp. – a group of relatively rare satellite trematodes collected from a raccoon gut. Credit: SB Weinstein.

Weinstein and her colleagues found that the data divided raccoon gut parasites into two distinct groups.


Top graph. Parasite frequency across raccoon populations. Most parasite genera were found in less than 10% of the raccoon populations.  Dashed line indicates 30% cutoff between satellite and core genera.  Bottom graph. Proportion of raccoons infected with each parasite  in relation to range-wide prevalence.  Larger data points indicate more populations surveyed for a given parasite.


There were eight taxa (genera) that were found in more than 40% of raccoon populations. In contrast there were 51 genera that were found in fewer than 30% of raccoon populations, with the vast majority of these found in fewer than 10% of raccoon populations in the survey (top graph on left).  The eight common taxa – core parasites – also tended to be present in more individuals within each population than did the 51 less common genera of satellite parasites (bottom graph on left).


Having defined core and satellite parasites, the researchers then did a thorough analysis of the gut contents of 180 raccoon collected by trappers and animal control agents in Santa Barbara County between 2012 – 2015. They hypothesized that the prevalence of core parasites should not be overly affected by ecotones.  In contrast, satellite parasites should increase in ecotones, because ecotones provide unique environmental conditions that would be suitable to some of the less common species in the parasite community.


In Santa Barbara County, Weinstein and her colleagues identified four core parasites and nine satellite parasites within the population, with a mean of 2.24 parasite species per raccoon. Racoons nearer to the marine ecotone harbored more parasite species than did raccoons more distant from the marine ecotone, a result of much greater richness of satellite species (left graph below). The story was very different for the freshwater ecotone.  Overall, parasite richness was relatively constant in relation to distance from the freshwater ecotone.  There were actually fewer core parasites but more satellite parasites near the freshwater ecotone (right graph below).


Left graph. Total parasite richness (orange line) in relation to distance from shore.  Satellites (orange fill) increased in abundance near the shore, while core parasites (maroon line) were steady. Right graph. Total parasite richness in relation to distance from freshwater.

Why did core parasite richness decline near the freshwater ecotone?  Weinstein and her colleagues believe that diet may play an important role.  For example, the core parasites Atriotaenia procyonis and Physoloptera rara were more common in raccoons far from freshwater, probably because racoons are infected by these two parasites as a result of eating terrestrial (but not aquatic) insect species that are intermediate hosts for these two parasite species.  As it turns out, these intermediate insect hosts prefer upland habitats that tend to be located relatively distant from the freshwater ecotone.

Increased abundance of rare parasites at ecotones has important implications for human health.  Several emerging infectious diseases, such as lyme disease, yellow fever and Nipoh virus are associated with ecotones. Habitat development by the expanding human population is causing increased habitat fragmentation, creating more ecotones, and potentially increasing the prevalence of these and other, equally unfriendly, parasites.

note: the paper that describes this research is from the journal Ecology. The reference is Weinstein, S. B., J. C. Van Wert, M. Kinsella, V. V. Tkach, and K. D. Lafferty. 2019. Infection at an ecotone: cross-system foraging increases satellite parasites but decreases core parasites in raccoons. Ecology 100(9):e02808. 10.1002/ecy.2808.  Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.


Forest canopy fixes nitrogen shortage

The two billion hectares of forest canopy remaining on our planet are ideal habitat for nitrogen fixing microorganisms that can convert N2 to ammonia.


View of the forest canopy at the research site. Credit: D. Stanton.

The forest canopy tends to be nutrient-poor because there is no access to nutrients that accumulate in the soils on the forest floor, and rainfall can leach away any nutrients that do accumulate in the canopy from atmospheric deposition. So if you are a microbe, and you want to enjoy the view from the canopy, it is to your advantage to be able to fix atmospheric nitrogen so you can build essential molecules such as proteins and ATP.

As I mentioned in a previous post (Nitrogen continues to confound convention) both phosphorus (P) and molybdenum (Mo) are essential nutrients for biological nitrogen fixation.  Daniel Stanton and his colleagues hypothesized that nitrogen fixation in the canopy might be limited by the availability of P and Mo, so they designed a series of experiments to explore the role of these nutrients at the San Lorenzo Canopy Crane in San Lorenzo National Park in the Republic of Panama.  The crane provides about 1 ha of canopy access to non-acrophobic ecologists.


The crane at the research site: Credit: D. Stanton.

In one experiment, Stanton and his colleagues filled thin nylon stockings with vermiculite to form 40 cm long cylinders of 4 cm diameter.  Each cylinder was then soaked in either pure water (control), a molybdenum (Mo) compound, a phosphorus (P) compound, or a combination of Mo and P,  thus establishing four treatments. They attached each of these stockings to five different trees and allowed them to reside in the canopy for six months, to be colonized by microorganisms.


Nylon stockings treated with nutrients (or untreated controls) and affixed to branches in the canopy. Credit: D. Stanton.

The researchers measured the rate of nitrogen fixation by cutting a 50 cm2 rectangle from the area of densest growth on each stocking, and incubating it (along with the colonizing microorganisms) in a closed bottle that they had inoculated with heavy nitrogen (15N).  They then measured how much 15N the colonizers took up during a 12 hr incubation period.


Samples incubating for 12 hr to measure the rate of nitrogen fixation. Credit: D. Stanton.

The most common colonizers were nitrogen fixing filamentous cyanobacteria. These cyanobacteria fixed nitrogen at a somewhat (but not statistically significant) higher rate with Mo addition and at a much higher rate with P addition, and even more so with Mo + P addition.


Nitrogen fixation rates for each experimental treatment. C = control.  Note that the y-axis is logarithmic, so these differences in fixation rates are substantial.  Non-overlapping lowercase letters above the bars indicate significant differences between the means.

Nitrogen fixation is complex and costly.  Part of the complexity arises because nitrogenase, the enzyme that catalyzes the reaction, cannot tolerate oxygen.  To deal with this problem, cyanobacteria have evolved heterocysts, which are specialized anaerobic cells where nitrogen fixation occurs.  How does nutrient addition influence heterocyst abundance and function?

There are actually two aspects to this story.  One finding is that Mo addition had no effect on heterocyst abundance, while P addition had a pronounced effect.


Heterocyst frequency for each experimental treatment.

A second aspect is that Mo addition had a pronounced effect on the efficiency of nitrogen fixation.  For one analysis the researchers compared the nitrogen fixation rate per heterocyst for the phosphorus addition treatments either without or with Mo addition (in other words, they compared the P added treatment to the Mo + P treatment). Nitrogen fixation rates were much higher in the Mo + P treatments.  So while Mo does not increase heterocyst abundance, it does dramatically increase heterocyst fixation efficiency.


Quantity of N fixed per heterocyst per day in relation to absence (left bar) or presence (right bar) of Mo.  P was added for both treatments.  Dark horizontal lines are the median values, quartile range is represented by top and bottom of each box, and the whiskers represent the range of values for each treatment.

Phosphorus acts by markedly increasing the overall cyanobacterial growth.  It increases the amount of cyanobacteria that colonizes the canopy and also increases heterocyst density per filament. In contrast molybdenum’s effect is more nuanced as it increases the efficiency of the nitrogen fixation reaction without having any (obvious) effect on cyanobacterial structure.

How do these findings influence our understanding of tropical forests in the western hemisphere?  It turns out that episodes of nutrient addition actually happen in nature, courtesy of vast plumes of nutrient-rich rock-derived dust that periodically blow over the Atlantic Ocean from the Sahara desert in western Africa. Preliminary estimates by Stanton and his colleagues indicate that nutrient enrichment from these dust plumes is sufficient to  profoundly increase the rates of nitrogen fixation in tropical forests.  This may require us to reconsider our understanding of how nitrogen cycles within and between ecosystems.

note: the paper that describes this research is from the journal Ecology. The reference is Stanton, D. E., S. A. Batterman, J. C. Von Fischer, and L. O. Hedin. 2019. Rapid nitrogen fixation by canopy microbiome in tropical forest determined by both phosphorus and molybdenum. Ecology 100(9):e02795. 10.1002/ecy.2795. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.