Tropical trophic cascade slows decomposers

In the rough and tumble natural world, consumers such as lions, lady bugs, llamas and lizards get most of the press, while producers such as peas, pumpkins and phytoplankton come in a close second.  Consumers earn their name because they get their energy from consuming other organisms, while producers produce their own energy (using photosynthesis or chemosynthesis) from inorganic molecules.  Often ignored in this ecosystem structural scheme are decomposers, which get their energy from breaking down the tissue of dead organisms.  They should not be ignored.  Much of the energy transferred through ecosystems passes through decomposers.

One reason they are overlooked is that most decomposers are tiny. Some of the largest decomposers are detritivores, which actually eat the dead materials (detritus), in contrast to other microbial decomposers such as bacteria and fungi.  Shredders are detritivores commonly found in streams and rivers; these aquatic insects eat portions of dead leaves and, in the process, shred them into much smaller pieces that energize other decomposers. Many researchers had noted that shredders were relatively rare in tropical streams, in part because there are many other larger consumers in the ecosystem that are willing to eat dead leaves and any shredders associated with them. Thus Troy Simon and his colleagues expected that shredders, such as the caddisfly, Phylloicus hansoni, would play, at best, a minor role in the streams they studied in the Northern Range Mountains in Trinidad.


A typical headwater stream located in the Northern Range mountains of Trinidad. Waterfalls in the uppermost reaches of these streams act as a barrier to the upstream movement of guppies, but not killifish and crabs, which can move over land during periods of heavy rain. Credit: Joshua Goldberg.

We will discuss interactions between several species in these aquatic systems.  Trees are important producers as they shed leaves into the streams; these leaves are broken down by shredders such as the aforementioned caddisflies and also microbial decomposers.   The major consumers are omnivorous crabs, Eudaniela garmani, which eat leaves and caddisflies (and many other items), and two fish species. Killifish, Anablepsoides hartii, eat caddisflies, other invertebrates and also the occasional small fish (including fish eggs).


Hart’s killifish (Anablepsoides hartii) are primarily insectivorous and major consumers of leaf‐shredding caddisflies. Credit: Pierson Hill.

Guppies, Poecilia reticulata, are much smaller than killifish, maxing out at 32 mm long in comparison to the killifish maximum length of 100 mm.  But guppies are much more omnivorous, feeding on leaves, leaf-shredding insects and even killifish eggs and larvae.


Male (left) and female (right) Trinidadian guppy (Poecilia reticulata). Guppies are omnivorous, feeding broadly on detritus as well as plant and animal prey, including young killifish. Credit: Pierson Hill.

Amazingly, killifish can disperse over land, as can crabs (less amazingly).  This allows them to bypass barrier waterfalls during wet periods, which results in them being the only large consumer species above waterfalls in many Trinidad streams.  Guppies lack killifish dispersal abilities, so they are often confined to stream reaches below significant waterfalls.  These species, and their consumption patterns are highlighted in the figure below.


Diagram of the two detrital-based food webs.  Above the waterfall is the KC reach, named after its two important consumers, killifish and crabs.  Below the waterfalls is the KCG reach, named after its three important consumers, killifish, crabs and guppies. Arrows show direction of energy flow within the ecosystem.

Simon and his colleagues wanted to know how interactions among all of these species influenced the rate of leaf decomposition.  The researchers constructed identical-size leaf packs of recently fallen leaves of the Guarumo tree, Cercropia peltata, and attached them to copper wire frames within each reach of the stream.  They periodically harvested a subset of the packs and measured the amount of decomposition by drying and weighing the leaves, and comparing this weight to the starting weight of the leaf pack.  In addition, they collected all invertebrates > 1 mm long from each leaf pack and identified them to species or genus.

To control the consumers involved in each interaction, Simon and his colleagues constructed underwater electric exclosures which created an electric field that convinced all fish and crabs to exit (and stay out) within 30 seconds of being turned on, but did not influence invertebrates in any detectable way.  Killifish are active day and night, guppies only during the day, and the researchers believed that crabs were active primarily at night. The researchers set up four treatments: control (C) with 24 hour access to consumers, experimental (E) with 24 hour exclusion of consumers, day-only exclusion (D) and night-only exclusion (N).  The researchers expected that the day-only exclusion treatments would selectively exclude guppies, while night-only exclusion would selectively exclude crabs. They then placed the leaf packs into each exclosure, turned on the current, and ran the experiment for 29 days.  Five replicates of each treatment were done above and below the waterfalls.


Electric exclosures established in the stream. Leaf packs were tied to the copper frame and periodically harvested over the 29 days of the experiment. Rectangular tiles shown in treatment frames were part of a separate study. Credit: Troy N. Simon.

We’re finally ready for some data.  The two graphs on the left represent the downstream reach below the waterfalls, where killifish, crabs and guppies are naturally present (KCG).  The two graphs on the right represent the upstream reach above the falls, where only killifish and crabs are naturally present.  There was no evidence in the downstream reach that excluding consumers influenced decomposition rates (top left graph).  However, when consumers were present (C treatment) in the upstream reach, decomposition rates were reduced by about 40% in comparison to treatments when consumers were partially (D and N) or completely (E) excluded (top right graph).


Mean (+SE) for (a,b) decay rate of Cecropia peltata leaves (percentage of mass lost per day) and (c,d)  biomass of Phylloicus hansoni (milligrams of dry mass per gram of Cecropia). 24-hour treatments allow full macroconsumer access [control (C)] or completely exclude macroconsumers [electric (E)]. Twelve-hour treatments exclude access to either diurnally active [day (D)] or nocturnally active [night (N)] macroconsumers. Different letters above the bars indicate statistically significant differences between the treatments.

The two bottom graphs above look at the biomass of the caddisfly, Phylloicus hansoni, which was easily the most abundant macroinvertebrate within the leaf packs.  There was no significant difference in caddisfly abundance below the waterfall regardless of treatment (bottom left graph above).  Above the waterfalls, caddisfly abundance was severely depressed in the controls (C) where killifish were free to feed on them (bottom right graph).

One piece of evidence that killifish ate caddisflies and depressed their abundance was that surviving caddisflies were much smaller in the control treatment leaf packs than in any of the experimental treatment leaf packs.  This suggests that  killifish with unimpeded access to caddisflies were picking off the largest individuals.


Mean (+SE) caddisfly length in mm (y-axis) for each treatment, 

These findings support the hypothesis that a trophic cascade prevails in the KC reach, in which killifish eat caddisflies, thereby slowing down decomposition. But in the KCG reach, guppies eat killifish eggs and larvae and compete with them for resources, thereby reducing killifish abundance, and interfering with the establishment of a trophic cascade.

Lastly, the researchers explored whether the same trophic cascade operated in upper reaches but not in lower reaches of other streams in the area. Surveys of six streams indicate a definite “yes” answer, with Cecropia decay rate and caddisfly biomass much lower in the upper reaches.


(Top) Mean (+SE) decay rate for Cecropia peltata
leaves (percentage of mass lost per day) and (b) caddisfly biomass (milligrams of dry mass per gram of Cecropia) in the landscape study (n = 6 streams). Different letters above bars indicate statistically significant differences  between treatments.

Surveys of each stream indicated that killifish were much more abundant in the upper reaches where guppies were not found, but guppies were much more prevalent in the lower reaches than were killifish.  These findings indicate that this detrital-based trophic cascade, with killifish eating caddisflies and thereby slowing down decomposition, is a general pattern in the upper reaches of these tropical streams.  However, Simon and his colleagues caution us that different streams will have different groups of organisms playing different ecological roles.  Thus the presence of detrital-based trophic cascades will depend on the particulars of which species are present and how abundant they are in a particular stream.

note: the paper that describes this research is from the journal Ecology. The reference is Simon, T. N., A. J. Binderup, A. S. Flecker, J. F. Gilliam, M. C. Marshall, S. A. Thomas, J. Travis, D. N. Reznick, and C. M. Pringle. 2019. Landscape patterns in top-down control of decomposition: omnivory disrupts a tropical detrital-based trophic cascade. Ecology 100(7):e02723. 10.1002/ecy.2723. 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.