Invading hippos

Jonathan Shurin was studying declining water quality in Lago de Tota, Colombia’s largest lake, when he learned about a local invasion of the common hippopotamus, Hippopotamus amphibius.  Four hippos were imported to Colombia by the notorious drug lord Pablo Escobar to populate his private zoo.  Following Escobar’s shooting death in 1993, the zoo fell into disrepair and the hippos wandered off free.  The population now numbers between 65-80, and breeding individuals have been seen 150 km from the zoo.


Hippos wallow in a lake framed by cattle egrits. Credit J. Shurin

Common hippos are native to central and southern Africa; as their scientific name implies they divide their existence between land (mostly at night) and water (keeping cool during the day).  These are huge animals, weighing up to 1500 kg and capable of running a surprising 30 kg/hr.  Apparently it is very easy to annoy a hippo.  From an ecosystem standpoint, hippos in their native Africa have been shown to have a strong impact on ecosystems by grazing on land at night and then releasing processed nutrients into lakes during the day.  Their influence is greatest during the dry season when they’re concentrated at high densities.  Jonathan Shurin and his colleagues wanted to know whether hippos were having a discernable effect on lakes and rivers in Colombia.  Given an expectation that the hippo population will continue to grow, this question has important management implications.


A grazing hippo. Credit: J. Shurin

The researchers sampled 14 small lakes at Hacienda Napoles in Antioquia, Columbia during the wet season and the dry season.  All lakes were sampled from shore because entering a lake containing hippos can be hazardous to a researcher’s health.peligrohippo

Two lakes were found to contain hippos, while the other 12 did not (though some had been observed with hippos on other occasions).  The analysis compared the two lakes with hippos to the 12 lakes without hippos for nutrients, conductivity, pH, temperature and chlorohyll-a concentration (a measure of photosynthetic activity).  The researchers sampled for phytoplankton, zooplankton and used dip nets to sample macroinvertebrates.  They found few differences in most categories except for the composition of the phytoplankton community. As you can see below, lakes with hippos had considerably more cyanophytes (photosynthetic bacteria often associated with harmful algal blooms), and fewer chlorophytes and charophytes (types of green algae) than did lakes without hippos.


Mean relative density of different divisions of phytoplankton in the two lakes with hippos (left bar) and the 12 lakes without hippos (right bar).

Shurin and his colleagues also estimated net production of each lake by systematically measuring dissolved oxygen concentration throughout the day. Photosynthetic organisms in highly productive lakes should take up lots of carbon dioxide during the day, and release considerable oxygen into the water.  Thus the difference in oxygen levels during the day (when photosynthesis occurs) vs. night (when there is no photosynthetic activity) would be greatest in highly productive lakes. The researchers discovered from multiple samples that the two lakes with hippos had an average range of 3.6 mg/L in dissolved oxygen levels which was significantly greater than the average range of 2.1 mg/L measured in three of the lakes without hippos (it was not feasible to measure all of the no hippo lakes). Presumably, this difference occurs from high photosynthetic rates during the day in the lakes with hippos.


Time series of dissolved oxygen in the sampled lakes.  Notice how dissolved oxygen levels peak in the late afternoon (hour 12 = noon), but decline overnight without input from photosynthesis.

In addition to comparing the quantity of nutrients, Shurin and his colleagues wanted to know the source of the nutrients.  Stable isotopes are forms of elements (in this case carbon and nitrogen) that differ in number of neutrons.  They are called stable, because they don’t undergo radioactive decay.  Stable isotope analysis measures the ratio of rare isotopes of a particular element in comparison to the more common isotope (for example 13C compared to 12C). Relevant to the hippo study, plants growing on land tend to have a higher (less negative for carbon, more positive for nitrogen) stable isotope ratio of carbon (delta13C) and nitrogen (delta15N) than do plants growing in water.  So if hippos were bringing nutrients into the lakes, the researchers expected the two hippo lakes to have higher stable isotope ratios of carbon and nitrogen.

As you can see from the graph below, on average, the two hippo lakes had higher stable isotope ratios of carbon, but not of nitrogen.  This indicates that hippos are importing carbon into the lake – presumably eating 13C rich plants during the evening, and then pooping out the remains when they return to the water.  However there is no evidence that hippos are importing nitrogen into the lakes.


Stable C and N isotopic ratios for samples collected from lakes with (green) and without (orange) hippo populations. Solid circles are the mean values of multiple samples collected at different times from the same lake, and open circles are the individual observations from each sample.

Shurin and his colleagues acknowledge the difficulty of drawing conclusions on ecosystem impact based on only two lakes with hippos.  On the other hand, finding significant differences with such a small sample is noteworthy, particularly when considering that the hippo invasion may be in its early stages.  If we extrapolate, from four hippos in 1993 to the lower estimate of 65 hippos at the time of the study, and assume exponential growth, we should find 785 hippos by 2040 and over 7000 hippos by 2060.  There are several assumptions with this extrapolation, but if unchecked the hippo population could expand dramatically, impacting ecosystem functioning in many different ways.


Observed (solid circles) and projected (open circles) growth of the hippo population in Antioquia, Columbia, assuming exponential growth.

But should we worry about this?  After all, hippos are amazingly cool, and tourists have begun visiting Hacienda Napoles specifically to see the hippos.  This is an example of a social-ecological mismatch, where the societal value placed on a species may oppose potential negative environmental impact. Conservation ecologists will need to work with the local community to devise a plan that serves the best interests of the ecosystem, and the humans who live there.

note: the paper that describes this research is from the journal Ecology. The reference is Shurin, J. B., Aranguren-Riaño, N., Duque Negro, D., Echeverri Lopez, D., Jones, N. T., Laverde‐R, O., Neu, A., and Pedroza Ramos, A. 2020. Ecosystem effects of the world’s largest invasive animal. Ecology 101(5):e02991. 10.1002/ecy.2991. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2020 by the Ecological Society of America. All rights reserved.

Nitrogen continues to confound convention

Ah nitrogen…  It is the most abundant molecule in the air that we breathe (close to 80%), yet plants always seem to be starving for it.  Annually, nitrogen fertilizers are a $75 billion dollar industry. The problem is that the nitrogen gas that we breathe (N2) is very nonreactive, because the two nitrogen atoms are held together by a massively powerful triple bond.  So N2 must be broken down to some other more usable form (such as ammonia) – a process we call nitrogen fixation.  Most nitrogen fixers are microorganisms that live in soils or symbiotically within plants.  Unfortunately, N-fixation is energetically very costly, so even organisms that can fix nitrogen will generally happily use nitrogen compounds from the soil or leaf litter (the layer of fallen leaves above the soil) if they are available, rather than expending enormous energy to fix it for themselves. The general formula for nitrogen fixation (ignoring protons, electrons and energy transfers) is…


A few years ago Scott Morford, Benjamin Houlton and Randy Dahlgren (the first two are co-authors of the present study) stunned the ecological world by identifying a previously unsuspected source of nitrogen – weathering of bedrock such as the mica schist pictured below. This bedrock was formed from seabeds which were rich in organic matter and had a high concentration of nitrogen compounds When the rock breaks down, both carbon and nitrogen compounds leach into the soil. Katherine Dynarski became interested in nitrogen fixation as an undergrad at Villanova University, so it was natural for her to move to the University of California at Davis to begin her graduate work with Morford and Houlton on how nitrogen cycles through ecosystems.


Nitrogen-rich mica schist bedrock. Credit: Katherine Dynarski.

Dynarski got involved in this specific project essentially by accident. She was helping a fellow graduate student collect rocks at adjacent forests on contrasting bedrock (one high-N mica schist, and one low-N basalt), and figured that while she was out there, she might as well measure some N-fixation rates. In leaf litter and the soil below, most N-fixation is done by free-living soil bacteria. Dynarski expected higher N-fixation rates in the litter collected above the N-poor bedrock, reasoning that the microorganisms would need to fix nitrogen from the air, because there was little present in the litter.  In contrast, she expected to find lower N-fixation rates in litter collected above the N-rich bedrock, reasoning that the micro-organisms could save considerable energy by using existing nitrogen that had leached into the soil and leaf litter layer. She was shocked when she ran the samples and found exactly the opposite of her expectation, which led her to develop a more substantial project looking at the relationship between bedrock and N fixing microbes.


Katherine Dynarski conducting gas incubations to measure N-fixation rates in the field. Credit: Scott Mitchell.

Working in northern California and Western Oregon, Dynarski and her colleagues identified sites whose bedrock was low in nitrogen (below 500 parts per million N) or high in nitrogen (above 500 ppm N). The researchers used soil and leaf litter samples from 14 paired sites – high N bedrock with nearby low N bedrock. They analyzed soil and leaf litter samples from each plot for concentration of nitrogen, carbon (C), phosphorus (P) and molybdenum (Mo) – the latter two elements have been shown in other systems to limit the rate of N-fixation.  The researchers also collected samples of underlying bedrock and analyzed N and Mo content of these rocks.

Recall that the conventional paradigm is that microorganisms should have lower N-fixation rates in N-rich environments.  There was negligible N-fixation occurring in the soil, but considerable N-fixation in the leaf litter above.  Thus the conventional prediction was that N-fixation rates would be higher in leaf litter above low-N bedrock. As I mentioned previously, Dynarski found the exact opposite to be true in one site; would this unconventional finding be confirmed by the 14 sites explored in this study?

The answer is yes!  Considerably more N-fixation was detected in leaf litter above high N bedrock than in leaf litter above low N bedrock.


Mean leaf litter N-fixation rates and low-N and High_N bedrock sites.  Error bars are one standard deviation. P = 0.014.

You will notice the large error bars above the graph.  As it turns out, N-fixation rates vary dramatically – even on a very small spatial scale, which is why the researchers took multiple samples from each site. Some sample sites (hotspots) have unusually high rates of N-fixation.  These hotspots are also strongly correlated with high carbon concentration, with greater C in the leaf litter associated with much higher rates of N-fixation.


Litter N-fixation rates in relation to % soil carbon at N-fixation hotspots. Hotspots are defined as having fixation rates greater than 1 kg N per hectare per year.

Dynarski and her colleagues also discovered that, in general, leaf litter above high-N bedrock tended to have more C and P than did leaf litter above low-N bedrock.  Given this finding (along with the hotspot finding) we are now ready to explore the question of why microbes are expending more energy to fix nitrogen in regions where more nitrogen is naturally available.

The researchers considered two hypotheses.  First, it takes N to make N.  N-fixation is catalyzed by N-rich enzymes. It may be that leaf litter above low-N bedrock is too N-poor to provide microbes with enough nitrogen make these enzymes. So the additional nitrogen from high-N bedrock is just enough to allow microbes to produce the N-fixation enzymes.

The second hypothesis is that the litter above low-N bedrock is also low in C, P and Mo, all of which are required for N-fixation. Thus the positive effect of these nutrients overwhelms the negative effect of additional nitrogen on the rate of nitrogen fixation.  According to this hypothesis, the conventional paradigm of high nitrogen availability reducing the rate of N-fixation is correct, but other factors may be equally or more important in natural ecosystems.

Fortunately, this conundrum is easily resolved.  Dynarski and her colleagues took some leaf litter samples and added a small amount of nitrogen to them.  These N-additions significantly reduced N-fixation rates at both low and high bedrock N sites.  Thus environmental N does reduce biological N-fixation, but other factors, such as the availability of other essential nutrients, can overwhelm the inhibitory effect of environmental nitrogen in natural ecosystems


A Douglas fir forest in the Oregon Coast Range, where some of this research was conducted.  Credit: Katherine Dynarski.

The researchers conclude that nitrogen input from bedrock weathering leads to increased C storage and P retention, ultimately enhancing rates of N-fixation. About 75% of Earth’s surface is underlain by rocks with substantial N reservoirs, so we need to continue exploring the effects of weathering bedrock on ecosystem processes and functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Dynarski, K. A., S. L. Morford, S. A. Mitchell, and B. Z. Houlton. 2019. Bedrock nitrogen weathering stimulates biological nitrogen fixation. Ecology 100(8):e02741. 10.1002/ ecy.2741. 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.

Decomposition: it’s who you are and where you are

“Follow the carbon” is a growing pastime of ecologists and environmental researchers worldwide. In the process of cellular respiration, organisms use carbon compounds to fuel their metabolic pathways, so having carbon around makes life possible.  Within ecosystems, following the carbon is equivalent to following how energy flows among the producers, consumers, detritivores and decomposers. In soils, decomposers play a central role in energy flow, but we might not appreciate their importance because many decomposers are tiny, and decomposition is very slow.  We are thrilled by a hawk subduing a rodent, but are less appreciative of a bacterium breaking down a lignin molecule, even though at their molecular heart, both processes are the same, in that complex carbon enters the organism and fuels cellular respiration.  However. from a global perspective, cellular respiration produces carbon dioxide as a waste product, which if allowed to escape the ecosystem, will increase the pool of atmospheric carbon dioxide thereby increasing the rate of global warming. So following the carbon is an ecological imperative.

As the world warms, trees and shrubs are colonizing regions that previously were inaccessible to them. In northern Sweden, mountain birch forests (Betula pubescens) and birch shrubs (Betula nana) are advancing into the tundra, replacing the heath that is dominated by the crowberry, Empetrum nigrum. As he began his PhD studies, Thomas Parker became interested in the general question of how decomposition changes as trees and shrubs expand further north in the Arctic. On his first trip to a field site in northern Sweden he noticed that the areas of forest and shrubs produced a lot of leaf litter in autumn yet there was no significant accumulation of this litter the following year. He wondered how the litter decomposed, and how this process might change as birch overtook the crowberry.


One of the study sides in autumn: mountain birch forest (yellow) in the background, dwarf birch (red) on the left and crowberry on the right. Credit: Tom Parker.

Several factors can affect leaf litter decomposition in northern climes.  First, depending on what they are made of, different species of leaves will decompose at different rates.  Second, different types of microorganisms present will target different types of leaves with varying degrees of efficiency.  Lastly, the abiotic environment may play a role; for example, due to shade and creation of discrete microenvironments, forests have deeper snowpack, keeping soils warmer in winter and potentially elevating decomposer cellular respiration rates. Working with several other researchers, Parker tested the following three hypotheses: (1) litter from the more productive vegetation types will decompose more quickly, (2) all types of litter decompose more quickly in forest and shrub environments, and (3) deep winter snow (in forest and shrub environments) increase litter decomposition compared to heath environments.

To test these hypotheses, Parker and his colleagues established 12 transects that transitioned from forest to shrub to heath. Along each transect, they set up three 2 m2 plots – one each in the forest, shrub, and heath – 36 plots in all. In September of 2012, the researchers collected fresh leaf littler from mountain birch, shrub birch and crowberry, which they sorted, dried and placed into 7X7 cm. polyester mesh bags.  They placed six litter bags of each species at each of the 36 plots, and then harvested these bags periodically over the next three years. Bags were securely attached to the ground so that small decomposers could get in, but the researchers had to choose a relatively small mesh diameter to make sure they successfully enclosed the tiny crowberry leaves. This restricted access to some of the larger decomposers.


Some litter bags attached to the soil surface at the beginning of the experiment. Credit: Tom Parker.

To test for the effect of snow depth, the researchers also set up snow fences on nearby heath sites.  These fences accumulated blowing and drifting snow, creating a snowpack comparable to that in nearby forest and shrub plots.

Parker and his colleagues found that B. pubescens leaves decomposed most rapidly and E. nigrum leases decomposed most slowly.  In addition, leaf litter decomposed fastest in the forest and most slowly in the heath.  Lastly, snow depth did not  influence decomposition rate.


(Left graph) Decomposition rates of E. nigrum, B. nana and B. pubescens in heath, shrub and forest. (Right graph) Decomposition rates of E. nigrum, B. nana and B. pubescens in heath under three different snow depths simulating snow accumulation at different vegetation types: Heath (control), + Snow (Shrub) and ++ Snow (Forest) . Error bars are 1 SE.

B. pubescens in forest and shrub lost the greatest amount (almost 50%) of mass over the three years of the study, while E. nigrum in heath lost the least (less than 30%).  However, B. pubescens decomposed much more rapidly in the forest than in the shrub between days 365 and 641. The bottom graphs below show that snow fences had no significant effect on decomposition.


Percentage of litter mass remaining (a, d) E. nigrum, (b, e) B. nana, (c, f) B. pubescens in heath, shrub, or forest. Top graphs (a, b, c) are natural transects, while the bottom graphs (d, e, f) represent heath tundra under three different snow depths simulating snow accumulation at different vegetation types: Heath (control), + Snow (Shrub) and ++ Snow (Forest) . Error bars represent are 1SE. Shaded areas on the x-axis indicate the snow covered season in the first two years of the study.

Why do mountain birch leaves decompose so much more than do crowberry leaves?  The researchers chemically analyzed both species and discovered that birch leaves had 1.7 times more carbohydrate than did crowberry, while crowberry had 4.9 times more lipids than did birch. Their chemical analysis showed much of birch’s rapid early decomposition was a result of rapid carbohydrate breakdown. In contrast, crowberry’s slow decomposition resulted from its high lipid content being relatively resistant to the actions of decomposers.


Researchers (Parker right, Subke left) harvesting soils and litter in the tundra. Credit: Jens-Arne Subke.

Parker and his colleagues did discover that decomposition was fastest in the forest independent of litter type. Forest soils are rich in brown-rot fungi, which are known to target the carbohydrates (primarily cellulose) that are so abundant in mountain birch leaves.  The researchers propose that a history of high cellulose litter content has selected for a biochemical environment that efficiently breaks down cellulose-rich leaves. Once the brown-rot fungi and their allies have done much of the initial breakdown, another class of fungi (ectomycorrhizal fungi) kicks into action and metabolizes (and decomposes) the more complex organic molecules.

The result of all this decomposition in the forest, but not the heath, is that tundra heath stores much more organic compounds than does the adjacent forest (which loses stored organic compounds to decomposers).  As forests continue their relentless march northward replacing the heath, it is very likely that they will introduce their efficient army of decomposers to the former heathlands.  These decomposers will feast on the vast supply of stored organic carbon compounds, release large quantities of carbon dioxide into the atmosphere, which will further exacerbate global warming. This is one of several positive feedbacks loops expected to destabilize global climate systems in the coming years.

note: the paper that describes this research is from the journal Ecology. The reference is Parker, T. C., Sanderman, J., Holden, R. D., Blume‐Werry, G., Sjögersten, S., Large, D., Castro‐Díaz, M., Street, L. E., Subke, J. and Wookey, P. A. (2018), Exploring drivers of litter decomposition in a greening Arctic: results from a transplant experiment across a treeline. Ecology, 99: 2284-2294. doi:10.1002/ecy.2442. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.