Drought differentially diminishes ecosystem production

Sometimes, even the most carefully conceived experiment is thrown for a loop by Mother Nature.  Good scientists must embrace the unexpected.  Ellen Esch, David Lipson and Elsa Cleland set out to explore how plant communities responded to high, normal and low rainfall conditions.  The researchers set up rainfall manipulation plots that were covered with a clear plastic roof that would allow most light to pass through, but intercept all of the water.  They then reapplied the intercepted water, with each plot receiving either 50%, 100% or 150% of the fallen rain.  The plan was to simulate drought, normal and wet conditions. The natural world had other plans, however, as 2013-2016 were unusually dry years. Fortunately the researchers adjusted, by refocusing their question on how plant communities respond to severe drought  (50% of intercepted rainfall), moderate drought (100%) and normal rainfall (150%).


Herbaceous plant community being irrigated (notice the rainbow). Credit: Ellen Esch.

Esch and her colleagues set up their experiment at the San Diego State University Santa Margarita Ecological Reserve, which has a Mediterranean-type climate with mild, somewhat moist winters and hot dry summers.


Exotic grasses (here showing recently senesced Bromus madritensis) dominated the herbaceous sites. Credit: Ellen Esch

They wanted to know how climatic variability brought about by climate change would influence plant phenology (the timing of periodic ecological events), specifically green-up date (when plants begin turning green) and senescence date (when they turn brown and curtail photosynthesis). They expected that the native species, primarily sage-type shrubs, would be more drought-resistant than the exotic herbaceous vegetation, which was dominated by brome grass.  Climate change is predicted to increase climatic variability, which should increase the frequency and intensity of severe droughts (and also of unusually wet years).

An important measure of ecosystem functioning is its productivity – the amount of carbon taken up by an ecosystem, usually by photosynthesis.  More productive ecosystems have more energy available to feed consumers and decomposers.  More productive ecosystems also take up and store more carbon dioxide from the atmosphere, which can help reduce climate change. The researchers used a reflectance radiometer to calculate the Normalized Difference Vegetation Index (NDVI), which essentially calculates how green an area is, and is a good measure of productivity.  Esch and her colleagues hypothesized that drought would reduce overall ecosystem NDVI, but that native vegetation would be more buffered against the negative effects of drought than would the invasive exotic vegetation.


A student from a plant physiology class at San Diego State University measures NDVI. Credit: David Lipson

Each year from 2013 – 2016, the researchers set up 30 3X3 meter plots; 15 plots were dominated by exotic herbaceous species such as brome, and 15 plots had mostly native shrub species such as sage. Plots were treated the same, except for receiving either 50%, 100% or 150% of the fallen rain, which corresponded to severe drought, moderate drought and normal rainfall, respectively. Periodically, the researchers used a radiometer to measure NDVI for each plot.  They discovered that, as expected, drought reduced NDVI much more in the plots dominated by exotic herbaceous species (top graph below) than in the plots dominated by native shrubs (bottom graph).


NDVI on each measurement date for plots dominated by (top graph) exotic herbaceous species and (bottom graph) native shrub species. Red square = severe drought treatment, green circle = moderate drought, blue triangle = normal precipitation. Error bars = +/- 1 standard error.

What caused this difference in response to drought between exotic plant-dominated and native plant-dominated communities?  Mechanistically, the native shrubs have deeper roots than the exotic grasses, which may allow them to take up more water.  But how does this translate to differences in green-up date and senescence date?


A student measures stem elongation on a senescent native shrub, the black sage Salvia mellifera, near the very end of the growing season. Credit: Ellen Esch.

The researchers used two different NDVI measures to help answer this question.  Maximum NDVI is the greatest daily NDVI measure over the course of the growing season.  It is correlated with the maximum productivity of the plant community (at its greenest!).  In contrast seasonally integrated NDVI is a measure of productivity summed over the entire growing season.  Keeping those distinctions in mind, under extreme drought maximum NDVI was much lower in the exotic plots than the native plots.  But exotic plot performance increased with rainfall, so that under the wettest conditions (normal rainfall), exotic plot maximum NDVI was similar to native plot maximum NDVI (graph a below). However, when considered over the entire growing season, native plots were consistently more productive than exotic plots (graph c below).


Effect of rainfall on (a) maximum NDVI (top left), (c) seasonally integrated NDVI (top right), (b) green-up date (bottom left) and (d) senescence date (bottom right). Colors indicate dominant plot community composition (yellow = herbaceous, green = shrub) and point shape indicates growing season year (circle = 2013, square = 2014, diamond = 2015, triangle = 2016).

Phenology played an important role accounting for these differences in seasonally integrated NDVI.  At all rainfall levels, the native plant communities greened-up well before the exotic plant communities (graph b above). Exotic plants greened-up somewhat earlier as rainfall increased, while native plant green-up date was independent of rainfall. At all rainfall levels, native plots senesced about one month later than exotic plots, with increased rainfall delaying senescence in both native and exotic plant communities (graph d above).

Esch and her colleagues conclude that species composition (native shrub vs. exotic herbaceous plants) and drought both influence phenology and productivity in this important ecosystem. Climate change is predicted to increase the frequency of extreme droughts in this and other ecosystems.  Consequently, drought coupled with invasion by herbaceous species threatens to sharply reduce ecosystem productivity, which will decrease the food available for consumers and decomposers, and simultaneously reduce the amount of carbon dioxide taken up and stored by the ecosystem, thereby contributing to further climate change.

note: the paper that describes this research is from the journal Ecology. The reference is Esch, E. H.,  Lipson, D. A., and  Cleland, E. E.  2019.  Invasion and drought alter phenological sensitivity and synergistically lower ecosystem production. Ecology  100(10):e02802. 10.1002/ecy.2802. 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.

Turkey mullein trichomes gobble up protective pollen

I’m always amazed at how brilliant plants can be.  For example Billy Krimmel and Ian Pearse showed in 2013 that many plant species exude sticky substances that entrap small arthropods, thereby attracting predators, which then rid these plants of many herbivores that might otherwise consume their leaves or reproductive structures. Jennifer Van Wyk joined this research group (which included Laure Crova) in graduate school. They were hunting for predatory hemipterans (true bugs) for a different experiment, which involved looking for them on turkey mullein (Croton setiger). They found plenty of predators, but almost no prey.  This was puzzling; what were these predators eating?  Intrigued, the researchers swabbed the turkey mullein leaves for pollen and found relatively vast quantities of pollen trapped in the trichomes (hairlike protuberances) of the leaves. Much of the pollen was from other species, and the researchers suspected that the trichomes were removing pollen from pollinators (primarily bees) that came to visit. Presumably the predators, which included spiders, hemipterans and ants, were attracted to this highly nutritious pollen.


Turkey mullein with predaceous hemipteran on lower right leaf. Credit: Billy Krimmel – http://www.miridae.com/our-team

Van Wyk and her colleagues wondered whether pollen capture benefitted turkey mullein. If turkey mullein used pollen to attract predators, and predators ate herbivores, pollen extraction by trichomes would be an adaptation that formed part of turkey mullein’s defense strategy.  If this is true, supplementing turkey mullein with additional pollen should increase visitation by predators, and decrease herbivore abundance.  With fewer herbivores, the researchers predicted less leaf damage.


Turkey mullein with herbivore-damaged leaves

Supplementing turkey mullein with additional pollen presents its own set of problems – most importantly coming up with enough pollen – in particular pollen that predators want to eat (Van Wyk and her colleagues collected a pound of oak pollen, only to find that predacious bugs were not interested in it).  The researchers grew sunflowers in greenhouses, secured squash pollen from friends’ gardens and used tuning forks to vibrate pollen from tarweed flowers.

The researchers then set up experiments using 60 turkey mullein plants from one population in 2013 and 80 plants from another population in 2014. Nearby plants were paired up, with one member of the pair receiving 150 mg of supplemental pollen each week from mid-August to mid-September.  They surveyed all arthropods visible to the naked eye, and categorized each species as predator or herbivore based on its primary diet (many of the arthropods were actually omnivorous).

In accordance with expectations, predator abundance was substantially greater in the supplemented populations in both years of the study. Spiders showed the most consistent increase, while Orius (the minute pirate bug) increased significantly in the 2014 population. The 2014 population had fewer arthropods of all species, possibly because it was immediately adjacent to an agricultural field.


Mean predator abundance per plant in 2013 (top) and 2014 (bottom). Geocoris is a Genus of big-eyed bugs, while Orius is the minute pirate bug. ** p < 0.01, † p < 0.1. Error bars are 1 standard error.

The results are less clear-cut with herbivore abundance.  Fleahoppers were 18% less abundant on supplemented plants in 2014, and slightly (not significantly) less abundant in supplemented plants in 2013.  Plants with a greater number of spiders had fewer fleahoppers, suggesting that spiders were eating them (or scaring them away). The researchers were unable to measure the abundance of an important herbivore, the grey hairstreak caterpillar, which forages primarily at night, and retreats into the soil during the heat of the day.


Mean number of fleahoppers  per plant in 2013 (left graph) and 2014 (right graph).  Blue bars indicated plants with supplemented pollen. * p < 0.05.

Lastly, supplemented plants suffered much less leaf damage than did unsupplemented plants.


Mean number of damaged leaves per plant in 2013 (left graph) and 2014 (right graph).  Blue bars indicated plants with supplemented pollen. ** p < 0.01.

Taken together, these experiments indicate that turkey mullein uses its trichomes to capture pollen and attract a diverse army of predators, which reduce herbivore abundance and reduce damage to the plant.  It is possible that pollen supplementation could be used on a larger scale to reduce herbivore loads on agricultural crops.  More generally, it will be interesting to see whether other plants with sticky trichomes, such as the marijuana plant Cannabis sativa, also use their trichomes to attract predators and reduce herbivore abundance.

note: the paper that describes this research is from the journal Ecology. The reference is Van Wyk, J. I.,  Krimmel, B. A.,  Crova, L., and  Pearse, I. S..  2019.  Plants trap pollen to feed predatory arthropods as an indirect resistance against herbivory. Ecology  100( 11):e02867. 10.1002/ecy.2867. 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.

Birds and plants team up and trade off

For many years, ecologists have been puzzling over the question of why the world is so green.  Given the abundance of herbivores in the world, it seems, on the surface, that plants don’t stand a chance. The famous naturalist/ecologist Aldo Leopold was one of the first scientists to emphasize the role of predators, which provide service for plants by eating herbivores (his example was wolves eating deer, ultimately preserving the plant community growing on a hillside).  As it turns out there are many different predator species providing these services. Colleen Nell began her PhD program with Kailen Mooney with a keen interest on how insectivorous birds locate their prey, and how this could affect the plants that are being attacked by herbivorous insects.

COYE common yellowthroat simple

 A Common Yellowthroat perches on Encelia californica. Credit: Sandrine Biziaux.

Plants are not as poorly defended as you might expect (having sat on a prickly pear cactus I can  painfully attest to that).  In addition to thorns and other discouraging structures, many plants are armed with a variety of toxins that protect them against herbivores.  Thorns and toxins are examples of direct defenses.  But many plants use indirect defenses that involve attracting a predator to the site of attack.  Some plants emit volatile compounds that predators are attuned to; these compounds tell the predator that there is a yummy herbivore nearby.  Nell and Mooney recognized that plant morphology (shape and form) could also act as an indirect defense, making herbivorous insects more accessible to bird predators. They also recognized that we might expect a tradeoff between how much a plant invests in different types of defense.  For example, a plant that produces nasty thorns might not invest so much in a morphology attractive to predaceous birds.


California Coastal Cactus Wren eating an orthopteran insect on a prickly pear cactus. Credit: Sandrine Biziaux.

What is a plant morphology that attracts birds?  The researchers hypothesized that birds might be attracted to a plant with simple branching patterns, so they could easily land on any branch that might be hosting a herbivorous insect (Encelia californica (first photo) has a simple or open branching pattern).  In contrast, birds might have a more difficult time foraging on insects that feed on structurally complex plants that host herbivorous insects which might be difficult to reach.

isocoma menziesii complex

Isocoma menziesii, a structurally complex plant. Credit: Colleen Nell.

The researchers chose nine common plant species from the coastal sage scrub ecosystem – a shrub-dominated ecosystem along the southern California coast. For each plant species they measured both its direct resistance and indirect resistance to herbivores.  Plants of each species were raised until they were four years old.  Then, for three months during bird breeding season, bird-protective mesh was placed over eight plants of each species, leaving five or six plants as unprotected controls.


Kailen Mooney and Daniel Sheng lower bird-protective mesh over a plant. Credit: Colleen Nell.

After three months, the researchers vacuumed all of the arthropods from the plants, measured each arthropod, and classified it to Order or Family to evaluate whether the arthropod was herbaceous.


Colleen Nell vacuums the arthropods from Artemisia californica. Credit: Colleen Nell.

Nell and Mooney evaluated the herbivore resistance of each plant species by measuring herbivore density in the bird-exclusion plants.  Relatively few herbivorous arthropods in plants that were protected from birds would indicate that these plants had strong direct defenses against herbivores.  The researchers also evaluated indirect defenses as the ratio of herbivore density on bird exclusion plants in comparison to controls (technically the ln[exclusion density/control density]).  A density of herbivores on plants protected from birds that is much greater than the density of herbivores on plants that allowed birds would indicate that birds are eating many herbivores. Finally, Nell and Mooney estimated plant complexity by counting the number of times a branch intersected an axis placed through the center of the plant at three different angles.  More intersecting branches indicated a more complex plant.

The researchers expected a tradeoff between direct and indirect defenses.  As predicted, as herbivore resistance (direct defense) increased, indirect defenses from birds decreased among the nine plant species.


Tradeoff between direct herbivore resistance and indirect defense by predaceous birds, for nine common plant species in the coastal sage scrub ecosystem.

The researchers also expected that more structurally complex plants would be less accessible to birds because complex branching would interfere with bird perching and foraging.  Thus Nell and Mooney predicted that structurally more complex plants would have weaker indirect defenses from birds, which is precisely what they discovered.


Indirect defenses (from birds) in relation to plant structural complexity .

Given that structurally complex plants received little benefit from birds, you might expect that they had greater direct defenses in the form of herbivore resistance.  Once again the data support this prediction.


Direct defenses (herbivore resistance) in relation to plant  structural complexity.

Initially, Nell was uncertain about whether increased plant complexity would deter insectivorous birds.  She points out that the top predators in this ecosystem are birds of prey that circle overhead in search of vulnerable birds to eat.  Structurally complex plants might provide refuge for insectivorous birds, which could result in them spending more time foraging in complex plants.  But the research showed the opposite trend. Plant complexity reduced the foraging efficiency of these small insectivorous birds, who prefer foraging on plants with relatively simple structure, which are easier to access and tend to host more prey.

note: the paper that describes this research is from the journal Ecology. The reference is Nell, C. S., and  Mooney, K. A..  2019.  Plant structural complexity mediates trade‐off in direct and indirect plant defense by birds. Ecology  100( 10):e02853. 10.1002/ecy.2853.  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.

Tadpoles shun trout across time

At a young school child (so long ago I can’t recall exactly when) I was exposed to Ernst Haeckel’s dictum that “ontogeny recapitulates phylogeny.”  More interested in language than biology at the time, I thought “cool – three words that I’m clueless about.” Though biological thinking about ontogeny – the processes of growth and development – has changed since Haeckel’s time, interest has, if anything, grown more intense across disciplines. Tiffany Garcia has explored her lifelong fascination with ontogeny by focusing her research on amphibians, which are famous for their distinct stages of development, each with unique habitats and ecological requirements. Working with eggs and tadpoles of the Pacific chorus frog (Pseudacris regilla), Garcia and her colleagues investigated whether stress associated with the presence of predators during one developmental stage (for example an egg) would carry over to influence behavior or development of subsequent stages.

chorus frog

The Pacific chorus frog (Pseudacris regilla). Credit Brett Hanshew.

A tadpole’s anti-predator strategy can be influenced by other factors besides carry-over from earlier developmental stages.  For example, we might expect that tadpoles whose ancestors lived in association with predators for many generations might have evolved a different anti-predator strategy than did tadpoles whose ancestors lived in a less threatening environment (this would be an adaptive effect). Tadpoles may also show very short-term changes in behavior or development (this is termed plasticity) if exposed to a cue that indicated a possible predation threat.


Collecting newly laid eggs at Three Creeks Lake. Credit: Lindsey Thurman

These three processes operate over very different time scales (long term – adaptive; intermediate term – carry-over; short term – plastic).  Garcia and her colleagues designed an experiment to explore how these processes might interact to influence a tadpole’s anti-predator strategy.  To investigate long term adaptive effects, the researchers collected newly laid (fertilized) eggs from lakes with and without rainbow trout (Oncorhynchus mykiss). They investigated carry-over effects by conditioning these eggs with four different environments during development: (1) trout odor, (2) cues from injured tadpoles (alarm cues), (3) trout odor paired with alarm cues, and (4) a water control (no odors nor cues).  The researchers created alarm cues by grinding up four juvenile tadpoles in 150 ml of water, and trout odor by housing 30 juvenile rainbow trout in a 200 L tank filled with well water.  They then conducted behavioral and developmental assays on tadpoles to see how adaptive, carry-over and plastic effects influenced tadpole growth, development and behavior.


Overview of the experimental design.

Garcia and her colleagues discovered that early exposure to trout odor had very little effect on growth and development, with body size and stage of development equivalent to that of controls.  In contrast exposure of eggs to tadpole alarm cues or to alarm cues + trout odor resulted in smaller, less developed fish (see table below).  In addition there was no effect of evolutionary history – eggs from lakes with and without trout showed similar patterns of growth and development.


Tadpole size and development in response to the four conditioning  treatments.  Higher Gosner stage numbers indicated more developed tadpoles. A tadpole hatches at Gosner stage 21 and begins metamorphosis at Gosner stage 42.

The next question is how do tadpoles respond behaviorally from exposure to different environments over the long, intermediate and short time scale?  To test tadpole anti-predator behavior, the researchers placed an individual tadpole into a tub that had a 6 X 8 cm piece of corrugated black plastic, which the tadpole could use as a refuge.  The researchers added to each tub one of the following: water (as a control (C)), tadpole alarm cues (AC), trout odor (TO), or alarm cues + trout odor (AC+TO).  After an acclimation period, a researcher noted the position of the tadpole (under the refuge or out in the open) every 20 minutes over a 3-hour time period.

There were no effects of evolutionary history on refuge use.  Tadpoles from lakes with and without trout showed similar patterns of refuge use.  However, embryonic conditioning to alarm cues and trout odor had a large effect on refuge use.  The left graph below shows the response of tadpoles from all four conditioning groups (C, AC, TO and TO+AC) to the addition of water.  As you can see, tadpoles that hatched from eggs that were conditioned with AC+TO were most likely to use refuges, while tadpoles from AC only or TO only eggs were somewhat more likely to use refuges. The pattern repeats itself when tadpole alarm cues are added to the water (second graph from left).  However when trout odor is added to the water, the responses are much more extreme, but follow the same pattern (third graph).  Lastly, when confronted with alarm cues and trout odor, tadpoles increase refuge use dramatically, but again show the same pattern, with tadpoles from control eggs using refuges the least, and tadpoles from eggs conditioned with alarm cues and trout odor using refuges the most (right graph).


Refuge use by tadpoles in response to embryonic conditioning and experimental exposure. C = water control, AC = tadpole alarm cue, TO = trout odor, and AC+TO = tadpole alarm cue and trout odor. Blue bars are means and gray bars are 95% confidence intervals.

There are two processes going on here.  First, over the short term, tadpoles are more responsive to the strongest cues, increasing refuge use when exposed to both tadpole alarm cues and trout odor.  Second, over the intermediate term, there is solid evidence for carry over effects.  Tadpoles that hatched from eggs conditioned with alarm cues and/or trout odor showed markedly increased refuge use than did tadpoles that hatched from control eggs.

These predator-induced responses impose a cost to the tadpoles.  Tadpoles exposed to alarm cues and trout odor while still in the egg were smaller and less developed, and probably metamorphosed into smaller frogs.  Many studies have shown that smaller frogs have reduced reproductive success.  The researchers recommend further studies to explore these trade-offs between survivorship, growth rate, development rate and size at metamorphosis. These studies are particularly essential, because rainbow trout are a non-native predator to these lakes.  Studies such as these allow conservation ecologists to understand the evolution and development of predator-prey interactions when novel species are introduced into an ecosystem.

note: the paper that describes this research is from the journal Ecology. The reference is Garcia, T. S.,  Bredeweg, E. M.,  Urbina, J., and  Ferrari, M. C. O..  2019.  Evaluating adaptive, carry‐over, and plastic antipredator responses across a temporal gradient in Pacific chorus frogs. Ecology  100( 11):e02825. 10.1002/ecy.2825.  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.

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.

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.


Hot ants defend plants from elephants

I’ve lost a lot of sleep over ants.  As a spider researcher, I often placed ants on spiderwebs to lure my spiders out of their underground retreats and onto their webs. The problem was that these harvester ants (Pogonmyrmex species) were fierce, so to minimize damage to myself, I was forced to capture them in the very early morning, when they and (alas) I were very sluggish.

acacias_thorn copy

Swollen thorn (domatia) that serves as living quarters for acacia ants. Credit: T. Palmer.

Todd Palmer has worked with ants for many years, including research on ant-plant mutualisms in which acacia trees provide domatia (swollen thorns) as ant living quarters and extrafloral nectaries as ant food, while ants provide protection from herbivores such as elephants, kudus and steenboks.

Similar to my efforts with ants and spiders, Palmer wanted to reduce ant-induced damage to himself and his colleagues, so he often took advantage of early morning ant sluggishness for purposes of manipulating acacia trees. On the other hand, if he wanted to study aggressive responses, he learned that mid-day was best. Recognizing the daily patterns of ant activity got Palmer, Ryan Tamashiro (Palmer’s undergraduate research student) and Patrick Milligan (Palmer’s graduate student) thinking about how these different levels of activity would influence herbivores, many of which tend to be most active during dawn and dusk when temperatures are low and ants are relatively sluggish.

Elephant side

Elephants are major herbivores that can cause enormous damage to acacia trees. Credit: T. Palmer.

Four species of ants live in domatia on branches of Acacia drepanolobium, the dominant tree species at Mpala Research Centre in Laikipia, Kenya.

Acdr habitat

A grove of Acacia drepanolobium. Credit: T. Palmer.

In order of relative abundance, the ant species are Crematogaster mimosae (52%), C. sjostedti (18%), Tetraponera penzigi (16%) and C. nigriceps (15%).  Previous research showed that C. mimosae and C. nigriceps are the two most effective acacia defenders.

Cnigriceps copy

Crematogaster nigriceps on an acacia tree. Credit: T. Palmer.

Ants are poikilotherms, whose body temperature, and presumably their activity levels, fluctuate with environmental temperature.  As these ants live in acacia branches, the first order of business became to determine how branch temperature fluctuated with time of day during the 21 days of data collection.  Not surprisingly, branch temperature peaked at mid-day, and was lowest at dawn and dusk (temperatures were not measured during the night).

TamashiroFig S!

Variation in branch surface temperature with time of day. Horizontal bars are median values; boxes are first and third quartiles.

Tamashiro, Milligan and Palmer next asked how ant activity level related to branch temperature.  Different ant species don’t get along so well, so each tree hosted only one ant species.  For each tree surveyed, the researchers counted the number of ants that passed over a 5 cm branch segment during a 30 second time period (they did this twice for each tree),  The researchers discovered a strong correlation between branch surface temperature and baseline ant activity, with C. mimosae and C. nigriceps showing greatest activity levels at all temperatures, which increased sharply at higher temperatures.

TamashiroFig 1a

Ant activity levels in relation to branch surface temperature. Shaded areas are 95% confidence intervals for each species.

Do higher temperatures cause a stronger aggressive response to predators or other disturbances? Tamashiro and his colleagues tested this by rapidly sliding a gloved hand over a 15 cm segment of a branch three times and then resting the gloved hand on the branch for 30 s.  They then removed the glove and counted the number of ants that had swarmed onto the glove.  Again, C. mimosae and C. nigriceps showed the strongest aggressive response, which increased sharply with temperature

TamashiroFig 1b

Aggressive swarming by ants in relation to branch surface temperature. Shaded areas are 95% confidence intervals for each species.

While a gloved hand is a nice surrogate for predators, the researchers wanted to know how the ants would respond to a real predator, and whether the response was temperature dependent.  At the same time, they wanted to determine whether the predator would change its behavior in response to changes in ant defensive behavior at different temperatures.  They used eight somali goats (Capra aegagrus hircus) as their predators, and C. mimosae as the focal ant species for these trials.

Cpl. Paula M. Fitzgerald, USMC - United States Department of Defense

Somali goats in Ali Sabieh, Djibouti. Credit: Cpl. Paula M. Fitzgerald, USMC – United States Department of Defense.

The researchers chose eight trees of similar size for their experiment, and removed ants from four of the trees by spraying them with a short-lived insecticide, and preventing ant recolonization by spreading a layer of ultra-sticky solution (Tanglefoot) around the based of each treated tree.  Goats were allowed to feed for five minutes.


Number of bites (top graph) and time spent feeding (bottom graph) by goats in relation to branch surface temperature. Shaded area is 95% confidence interval.

Tamashiro and his colleagues measured the number of bites taken (top graph) and the amount of time spent feeding (bottom graph) at different branch temperatures.  Both measures of goat feeding were not influenced by branch temperature if there were no ants on the trees (blue lines and points).  But if ants were present (red lines and points), goat feeding decreased sharply with increasing branch temperature, presumably reflecting more aggressive ant defense of the plants.

These findings have important implications for acacia trees, which are a critical species in the sub-Saharan ecosystem.  Previous research has shown that elephant damage is strongly influenced by the number of swarming ants on a particular tree; a greater number of swarming ants are associated with less elephant damage. Many vertebrate browsers feed throughout the day, but may feed preferentially at dawn and dusk, when temperatures are cooler and ant-defense is weakest. Browsing is particularly problematic for acacia saplings, which are usually attacked by small-bodied vertebrates such as steenbok, which forage primarily at night when ants are least active.  Thus the effectiveness of ant defense may be compromised by mismatches between vertebrate activity periods and ant activity periods.

note: the paper that describes this research is from the journal Ecology. The reference is Tamashiro, R. A., P. D. Milligan, and T. M. Palmer. 2019. Left out in the cold: temperature-dependence of defense in an African ant–plant mutualism. Ecology 100(6): e02712. 10.1002/ecy.2712 . 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.



Vacation’s changing tides

Cindy and I and our dog (Cheyanne) recently returned from a two+ week vacation at North Carolina’s Outer Banks.  We stayed in Avon, which is about eight miles north of the iconic Cape Hatteras lighthouse in a large house with a great ocean view.  We got a large house, because we thought our kids might join us, but it turns out that one disadvantage of kids getting older is that their lives become more complex.  Anyhow, several friends stayed with us for a few days, and a grand time was had by all.


Cheyanne and I ponder the ocean’s vastness. Credit: Cindy Miller

But the point of this post is the trip home.  On Friday, we packed everything into our car, including Cheyanne, and began the eight-hour drive back to our home in Radford, VA.  At Rodanthe (about 15 miles north), traffic just stopped.  We sat in our car for a few minutes, disembarked, and spoke with many people walking by, who told us that the road (NC12) was flooded and covered with sand.  We had heard rumors of flooding, but since the sun was out and the wind relatively calm, we assumed that was all in the past.  Apparently the flooding was so bad that a motor home and the boat it was towing got totally caught up in the sand and water, and was wedged so efficiently that they could not even be towed out until serious excavation happened. That was not going to happen until Saturday.


Moving the dunes off of the road. Credit: Cindy Miller.

Saturday at 6 PM we got the call that the road was open and we could head home.  We repacked the car, re-experienced Cheyanne’s baleful look, and set out, with an ETA of 3 AM at the earliest.  Alas the high tide came in, water breached the dunes, and a very kind police officer knocked on our window, imploring us to return to Avon and wait for a better day.  Cheyanne gave him a baleful look, but we obeyed.


Reconstituted dunes.  Notice the tire tracks left by earth-moving machines. Credit: Cindy Miller.

The next morning we set out again; by now we could pack a car in just a few minutes.  Our peanut butter on toast dinner of the previous night had left us a bit peckish, so we stopped off for some pastries and cappuccinos. We headed north once again and this time we were able to pass through the Rodanthe flood, and several others along the way.  The water level was high, but our car had good ground clearance and our escape was relatively uneventful, but done at sub-breakneck speed.


Riding away through Rodanthe’s rising tides. Credit: Cindy Miller.


Why was this happening?  The weather was beautiful – no rain, no wind and sunny skies.  It just doesn’t get any nicer than this at the Outer Banks.  As it turns out, there were two provocateurs.  First, there was subtropical storm Melissa several hundred miles to our east, passing harmlessly out to sea, but increasing sea levels.  Second, there was almost a full moon, which also tends to increase sea levels.  But that’s it!

That shouldn’t be enough.  In past years those two events might cause waves to crash to the dunes with increased vigor, but would not cause them to breach the dunes and spill onto the roads.  But those were past years, and now is the present, and sea levels along the North Carolina coast have risen by about one foot in the past 50 years.  Here are some data from Wilmington, NC – about 150 miles south of Avon.


Rising sea levels measured at Wilmington, North Carolina. Credit: National Oceanic and Atmospheric Administration and SeaLevelRise.org

You should note two things.  First, there is substantial year-to-year variation in sea levels. Second, rates of sea level rise are accelerating.  Scientists at the National Oceanic and Atmospheric Administration and the US Army Corps of Engineers expect this trend to continue.  Here is the prognosticated change in sea levels between now and 2050 at Oregon Inlet (just a few miles north of Rodanthe).


Forecast sea level change between 2016 and 2050. Credit: National Oceanic and Atmospheric Administration, U. S. Army Corps of Engineers and SeaLevelRise.org

This is very bad.  I’ve been vacationing at the Outer Banks for about 25 years; it has become a part of who I am.  I don’t want to give up on this spectacular part of the world, but we must act.  We cannot continue sticking our heads in the sand (which we can now oftentimes find on NC12), pretending that climate change is a construct of the liberal press or elite intelligentsia.

The first step in dealing with a problem is acknowledging that it exists. Climate change is here, and its impact is increasing. An estimated 50 million climate change refugees around the globe are being forced to abandon their homes. More will follow, including our neighbors from North Carolina’s Outer Banks. For their sake, and ours, let’s acknowledge the problem, and focus our resources, energies and talents to reducing the damage in the short term, and dealing with the causes of climate change over the next decades and centuries.

Mystifying trophic cascades

Within ecosystems, trophic cascades may occur when one species, usually a predator, has a negative effect on a second species (its prey), thereby having a positive effect on its prey’s prey. Today’s example considers the interaction between a group of predators (including several fish species, a sea snail and a sea star) their prey (the sea urchin Paracentrotus lividus) and sea urchin prey, which comprise numerous species of macroalgae that attach to the shallow ocean floor. These predators can negatively affect sea urchin populations either by eating them (consumptive effects), or by scaring them so they forage less efficiently (nonconsumptive effects). If sea urchins are less abundant or less aggressive foragers, the net indirect effect of a large population of fish, sea snails and sea stars will be an increase in macroalgal abundance.

Maldonado Halo

A large sea urchin grazing in a macroalgal community.  Notice the white halo surrounding the urchin, indicating that it has grazed all of the algae within that region. Credit: Albert Pessarrodona.

Many humans enjoy eating predatory fish, and we have overfished much of the ocean’s best fisheries including the shallow temperate rocky reefs (4 – 12 m deep) in the northwest Mediterranean Sea. Removing these predators has caused sea urchin populations to explode, overgrazing their favorite macroalgal food source, and ultimately leading to the formation of urchin barrens – large areas with little algal growth, low productivity and a small nondiverse assemblage of invertebrates and vertebrates.


A sea urchin barrens whose macroalgae have been overgrazed by sea urchins. Credit: Albert Pessarrodona

Albert Pessarrodona became interested in this trophic cascade after years of diving in the Mediterranean. He noticed that in Marine Protected Areas, predatory fish abound and there are few visible urchins and lots of macroalgae. In nearby unprotected areas where fishing is permitted, urchins graze out in the open brazenly, and urchin barrens are common. He also wondered whether a second variable – sea urchin size – might play a role in this dynamic. Were large sea urchins relatively immune from predation by virtue of their large size and long spines, allowing them to forage out in the open even if predators were relatively common?


Interactions investigated in this study.  (a) Predators consume either small (left) or large (right) sea urchins (consumptive effects). (b) Sea urchins eat macroalgae. (c) Predators scare small or large sea urchins, reducing their foraging efficiency (nonconsumptive effects). (d) Predatory fish indirectly increase macroalgal abundance.

Pessarrodona and his research team used field and laboratory experiments to explore the relationship between sea urchin size and their survival and behavior in high-predator-risk and low-predator-risk conditions. High-risk was the Medes Islands Marine Reserve, which has had no fishing since 1983 and boasts a large, diverse assemblage of predatory fish, while low-risk was the nearby Montgri coast, which has a similar habitat structure, but allows fishing. The researchers tethered 40 urchins of varying sizes to the sea bottom (about 5m deep) in each of these regions, left them for 24 hours, and then collected the survivors to compare survival in relation to body size in high and low-risk conditions. They discovered that large urchins were much less likely to get eaten than were small urchins, and that the probability of getting eaten was substantially greater in the high-risk site.


Probability of being eaten in relation to sea urchin size (cm) in high-risk (blue line) and low-risk (green line) habitats.

Pessarrodona and his colleagues followed this up by investigating whether the relatively predation-resistant large urchins were less fearful, and thus more likely to forage effectively, even in high-risk sites. Previous studies showed that sea urchins can evaluate risk using chemical cues given off by other urchins injured in a predatory attack, or given off by the actual predators. To explore the relationship between these cues and sea urchin behavior, the researchers put either large or small sea urchins into partitioned tanks with an injured sea urchin. Water flowed from one partition to the other, so the experimental sea urchins received chemical cues from the injured urchins. They also had a group of sea urchins placed in similar tanks without any injured sea urchins as controls. The experimental sea urchins were given seagrass to feed on, and the researchers calculated feeding rates based on how much food remained after seven days.

Small sea urchins were not deterred by the presence of an injured urchin (left graph below), while large sea urchins drastically reduced their feeding rates in response to the presence of an injured urchin (middle graph). This was startling as it flew in the face of the commonsense expectation that small sea urchins (most susceptible to predation) should be most fearful of predator cues. The researchers repeated the experiment (under slightly different conditions) placing an actual predator (a fearsome sea snail) on the other side of the partition. Again, large urchins showed drastically reduced foraging rates (right graph below).


Sea urchin responses to predation risk cues in the laboratory. When exposed to injured urchins – symbolized as having a triangle cut out – (A) small urchins did not reduce their grazing rate, while (B) large urchins drastically curtailed grazing. (C) When exposed to a predatory snail on the other side of a partition, large urchins sharply curtailed grazing. n.s = no significant difference, **P<0.01.

It turns out that large sea urchins are the critical players in this trophic cascade because they do much more damage to algal biomass than do the smaller urchins (we won’t go through the details of that research). The question then becomes how this plays out in natural ecosystems. Do consumptive and non-consumptive effects of predators in high-risk sites reduce sea urchin abundance and reduce the foraging levels of large sea urchins so that macroalgal cover is greatly enhanced? Pessarrodona and his colleagues surveyed high-risk and low-risk sites for sea urchin density and algal abundance. They set up 45 quadrats (40 X 40 cm) at each site, measured each sea urchin’s diameter, and estimated the abundance of each type of algae by harvesting a 20 X 20 cm subsample from each quadrat and drying and weighing the sample.

The findings were striking. Small and large sea urchins were much less abundant at high-risk sites than at low-risk sites (left graph below). At the same time, macroalgae were much more abundant at high-risk sites than at low-risk sites (right graph below).


(Left graph) Density of small and large sea urchins in high-risk and low-risk habitats. (Right graph) Biomass of macroalgae of different growth structures in high-risk and low-risk habitats. Canopy algae are taller than 10 cm, while turf algae are lower stature. Codium algae are generally not grazed by sea urchins. **P<0.01, ***P<0.001.


Summary of interactions.  Arrow width indicates relative importance.

To summarize this system, predators reduce small sea urchin abundance by eating them (consumptive effects), and reduce large sea urchin foraging by intimidating them (nonconsumptive effects). The net indirect effect of predators on macroalgae is a function of these two effects. Large sea urchins are the major macroalgae consumers, but, of course, large sea urchins develop from small sea urchins.

The $64 question is why large sea urchins fear predators so much, while small (more vulnerable) urchins do not. The quick answer is that we don’t know. One possibility is that small sea urchins may be bolder in risky environments since they are more vulnerable to starvation (have fewer reserves), and also have lower reproductive potential since they are likely to die before they get large enough to reproduce. In contrast, large sea urchins can survive many days without food because of their large reserves. In addition, large urchins are close to sexual maturity, and thus may be unwilling to accept even a small risk to their well-being, which could interfere with them achieving reproductive success.

note: the paper that describes this research is from the journal Ecology. The reference is Pessarrodona, A.,  Boada, J.,  Pagès, J. F.,  Arthur, R., and  Alcoverro, T. 2019.  Consumptive and non‐consumptive effects of predators vary with the ontogeny of their prey. Ecology  100( 5):e02649. 10.1002/ecy.2649. 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.