Stress frequency structures communities

COVID-19 has amplified our experience of stress, but even in a COVID-free world, we share with most other organisms a continuously stressful existence, highlighted by situations affecting our survival (e.g. getting food and not becoming someone else’s food) and our reproductive success.  Today we will discuss organisms that live in a very stressful environment – the subtidal zone off of the Galapagos islands – located just below the line demarcating the furthest extent of low tide.  One serious stress for subtidal organisms is coping with dramatically fluctuating ocean currents.  The speedy surgeonfish uses its powerful pectoral fins and slender, disc-shaped body to minimize drag, permitting feeding in high flow conditions brought about by powerful ocean waves.  In contrast, the broad-bodied torpedo-shaped parrotfish is unable to do so; for it, fast water is too much of a drag.

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Yellowtail surgeonfish (Prionurus laticlavius) stand out as voracious herbivores that can feed even in the most wave-swept coastlines of the Galapagos Islands. Credit: Dr. Alejandro Perez-Matus.

Waters near the Galapagos Islands are enriched by upwelling equatorial currents, which provide nutrients to a diverse community of plankton and benthic (attached to the ocean bottom) algae.  These in turn support a high diversity of macroinvertebrates and herbivorous fish that feed on them, including the pencil urchin, Eucidaris galapagensis, a voracious feeder on algae, barnacles and coral. This species wedges itself among rocks and crevices during the day, and emerges to feed at night.  It attaches itself (and moves very slowly) using its tube feet.  Robert Lamb, Franz Smith and Jon Witman hypothesized that given the weak attachment strength of the pencil urchin’s tube feet, it might only be an effective feeder in locations where wave action was minimal.

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Robert Lamb bolts experimental cages to the rock as Eucidaris urchins stand guard at the sheltered side of Caamaño. Credit: Salome Buglass.

To explore how wave action might affect the subtidal community, the researchers set up two research locations at Caamaño and Las Palmas – both off the Galapagos Island of Santa Cruz.

LambFig1

Effect of wave action (exposed – dark bar, sheltered – light bar) on abundance of some of the important members of the subtidal community off of the island of Santa Cruz.

 

At each location, they chose an exposed site with strong wave action and a sheltered site that had much reduced wave action.  Mean flow speed was more than twice as fast at exposed sites than in sheltered sites. As you can see in the figure to your left, site differences in mean flow speed corresponded to differences in the subtidal community. Crustose coralline algae (red algae firmly attached to corals) were more common in sheltered sites (Figure A), while a variety of red and green macroalgae were more common at exposed sites (Figure B).  Surgeonfish (Figure C) and parrotfish (Figure D) were much more abundant in exposed areas, while pencil urchins were much more abundant in sheltered sites (Figure E).

 

 

 

 

 

Lamb and his colleagues wanted to know why these differences exist. They set up a series of exclosures within each of these sites using wire mesh cages to either allow fish, but not urchins (+ fish treatment), allow urchins but not fish (+ urchins), or exclude both groups of herbivores (- all).  They also had a control treatment that allowed all herbivores (+ all).

LambTreatments

In one experiment the researchers created sandwiches made up of the delectable green algae Ulva.  For five days, they ran six replicates of each treatment at exposed and sheltered sites at Caamaño and Las Palmas. Lamb and his colleagues then harvested the sandwiches, weighed them, and calculated the percent remaining of each sandwich.

LambUlvaSandwich

An Ulva sandwich

At exposed locations, urchins (without fish) consumed very little Ulva, while fish (without urchins) consumed about 2/3 of the Ulva (when compared to the –all controls). In contrast, at sheltered locations, urchins took some mighty significant bites from the Ulva sandwiches, while fish also ate substantial Ulva at Caamaño, but not at Las Palmas.

LambFig3

Percent of Ulva biomass remaining after five days of the Ulva sandwich experiment. Error bars are 1 SE.

In a related experiment, the researchers used the same cages to explore how macroalgal communities assemble themselves in the presence or absence of urchin and fish herbiores under different flow rates.  If this was not enough to consider, they also ran these experiments both during the cool season, when nutrient-rich ocean currents lead to high production, and during the warm season when production is usually lower.  Lamb and his colleagues bolted two 13 X 13 cm polycarbonate plates to the bottom of each cage, and after two months measured the abundance and type of algae that colonized each plate.

Several trends emerge.  First, macroalgae colonized much more effectively during the cool season.  Second, urchins profoundly reduced macroalgal colonization at sheltered sites, but had little effect at exposed sites.  In contrast, fish herbivory reduced macroalgal colonization at exposed sites at Caamaño but not Las Palmas, during the warm and cool season.

LambFig4

Effect of herbivores on macroalgal community assembly, as measured by amount of algae colonizing the polycarbonate plates after two weeks.

In addition, the researchers set up video cameras and were able to document herbivory by 17 fish species, with drastically higher herbivory rates at exposed sites.

Lamb and his colleagues conclude that the dominant herbivores switched between urchins in low flow sites and fish in exposed sites. Fish can leave the resource patch when stress (flow rate) is unusually high, and return when flow rate drops, while the slow-moving pencil urchins do not have that option. The researchers argue that in many ecosystems, consumer mobility in relation to the frequency of environmental stress can predict how consumers influence community structure and assembly.  They point out that the coupling of mobility effects with environmental stress is common throughout the natural world.  As examples, many shorebirds feed on marine organisms that become available during low tides, or also between crashing waves.  Large mammals in Africa can migrate long distances to escape drought-stricken areas, while smaller animals cannot undertake such long journeys.  In locally acidic regions of the Mediterranean Sea, many fish species can enter, feed and leave before experiencing toxic effects from the acid water, while slow-moving urchins are excluded from feeding in those habitats. Thus, while extreme environmental stress often decreases consumer activity, there are also times when it doesn’t.  In these cases, we need to understand how particular species will behave and perform in the stressful environment to predict how stress influences community structure and functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Lamb, R. W.,  Smith, F., and  Witman, J. D..  2020.  Consumer mobility predicts impacts of herbivory across an environmental stress gradient. Ecology  101( 1):e02910. 10.1002/ecy.2910. 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.

Hot invaders thwart endemic New Zealanders

Tongariro National Park in New Zealand’s North Island is changing in many ways.  Over the past 50 years, the park, which has three large volcanoes, has increased in temperature at about three times the global average (about 1.5 deg. C) and is also receiving reduced annual rainfall. The park hosts a large number of endemic plants – species that are native to that region and found nowhere else.

GiejsztowtPark

Tongariro National Park in New Zealand.  The plastic sheets in the foreground are open top enclosures used to experimentally raise air and soil temperatures. Credit: Justyna Giejsztowt.

Monoao (Dracophyllum subulatum), is an endemic shrub that thrives in low-lying areas between the volcanoes.  Ecologically it is a facilitator, in that its growth form protects a variety of native species from heavy frosts, thereby promoting high species diversity within the plant communities.

GiejsztowtMonoao

The native monoao (Dracophyllum subulatum). Credit: Justyna Giejsztowt.

In addition to the threat of climate change, portions of Tongariro National Park are also being invaded by common heather (Calluna vulgaris), which has already caused a decline in many native and endemic plant species, and their associated insect communities.  Justyna Giejsztowt had worked previously as a technician for a project that investigated how climate change affected plant communities.  She noticed that the invasive heather had a stronger phenological response to warming than did the native community, flowering earlier and reaching peak floral density at an earlier date. Watching the countryside turn pink from the invasive flowers during that season, she wondered whether the pollinator community might be changing as well, which could affect the reproductive success of the surrounding native vegetation.  So she and her colleagues decided to do some experiments.

GiejsztowtHeather

The invasive heather, Calluna vulgaris. Credit: Justyna Giejsztowt.

Beginning in 2014, the researchers used hexagonal open-topped chambers to increase air and soil temperatures in experimental plots, while also maintaining unmanipulated control plots (you can see the plastic chambers in the top photo of Tongariro National Park). The researchers measured flowering dates for monoao and heather in each plot (and 11 other less abundant species as well), and estimated the number of flowers in each plot on a regular basis.

SITemoFif1

Daily mean temperatures (°C) over the 2015/2016 austral summer in experimentally warmed (red) and ambient temperature (blue) plots.

The researchers expected that experimental warming would cause more overlap between the time period when monoao and heather were both in flower.  This is exactly what they found.  Heather reached a high level of flowering much earlier in the year under experimental warming, increasing the percentage of flowering overlap from 2.79% (top graph below) to 11.27% (bottom graph).

GiejsztowtFig1A

Floral density of Calluna vulgaris (heather – dashed line) and Dracophyllum subulatum (monoao – solid line) under ambient (top graph) and experimentally warmed (bottom graph) temperature regimes. Shaded regions denote flowering overlap of monoao with high densities of heather.

This increase in overlap would increase the number of flowers open at a particular time, which might increase competition for pollinators leading to reduced reproductive success. On the other hand, increase in overlap could make a strong visual or olfactory impression on pollinators, drawing them into the area and thereby increasing plant reproductive success.  Or both forces could be important and cancel each other out.

Giejsztowt and her colleagues set up a second experiment to explore how the ratio of native monoao to invasive heather in a patch, and also the total number of flowers of either type within the patch, influenced monoao’s reproductive success.  They intentionally chose patches that had either (1) high monoao flower numbers and high heather flower numbers, (2) high monoao, low heather, (3) low monoao, high heather, or (4) low monoao, low heather.  The researchers chose nine focal plants within each plot, and from these plants they set up four transects running north, east, south and west. Each transect was 25 meters long and 40 cm wide.  The researchers estimated flower abundance in each transect.  As their measure of monoao reproductive success, they collected seeds produced by each focal monoao plant, dried them and then weighed them.

Giejsztowt and her colleagues found that neither the ratio of native to invasive plants, nor total floral density had any direct effect on monoao reproductive success.  However, the interaction of these two factors had a strong effect.  Seed masses of focal monoao plants were heaviest in patches with a high ratio of native to invasive plants, but only if the patches had intermediate or high overall floral density.  In contrast, monoao in patches composed of mostly invasive heather had consistently low seed masses, regardless of overall flower density in the patch.

GiejsztowtFig1B

Monoao seed mass (g) adjusted for the effect of plant height, relative to total floral density in the landscape. Colors denote native monoao (green) or invasive heather (black) dominance (making up more than 50% of the flowers). 

The researchers were not surprised to find that heather responded more strongly to increased temperature than did monoao, as several studies have shown that invasive species tend to have flexible phenology in response to changing environmental conditions. By shifting its peak flowering earlier in response to warmer temperature, heather increased its flowering overlap with monoao, which could, and did, increase competitive effects on monoao reproductive success.  When there were numerous flowers in a patch, but monoao was rarer than heather, monoao had relatively low reproductive success.  In contrast, if monoao was more common than heather, it achieved much greater reproductive success.

Why does this happen?  The researchers suggest that at high floral densities, heather may outcompete monoao for pollinators.  The mechanism for this competitive effect is unknown; invasive species have been shown to influence pollinator behavior and the numbers and types of pollinator within the community.  Because pollinators are declining globally, it is critical to understand how climate change and invasive species can interact to reduce pollination services to native plants within ecosystems.

note: the paper that describes this research is from the journal Ecology. The reference is Giejsztowt, J.,  Classen, A. T., and  Deslippe, J. R..  2020.  Climate change and invasion may synergistically affect native plant reproduction. Ecology  101( 1):e02913. 10.1002/ecy.2913. 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.

Warming Arctic forests diverge over nutrients

Humans continue their unique uncontrolled experiment to see how increased atmospheric carbon dioxide and the resulting warmer temperatures influence biomes worldwide.  One expected outcome of this global experiment is that trees in the extreme north will show improved growth resulting from a more benign physical environment.  As it turns out, some regions of the north do show this trend, while others don’t – this lack of consistent response is known as divergence.  For her graduate work, Sarah Ellison, working with Patrick Sullivan, Sean Cahoon and Rebecca Hewitt, wanted to document divergence in northern Alaska, and to figure out what might be causing it.

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The Wind River, near Arctic Village in the Arctic National Wildlife Refuge, is the easternmost site in the study. Credit: Patrick Sullivan.

The researchers established four study sites in four watersheds across the Brooks Range in northern Alaska.  They knew from previous studies that white spruce (Picea glauca) in the western Brooks Range have shown increased growth in response to climate warming, whereas those in the central and eastern Brooks Range have not responded. Some researchers hypothesized  that warmer temperatures caused moisture limitation in the eastern Brooks Range, but previous plant physiological studies done by this research team show no evidence of water stress, even in the extreme eastern portion of the range.

EllisonFig1

The four study sites within the Brooks Range from west to east: Agashashok, Kugururok, Dietrich and Wind River.

So what’s causing divergence?

At each study site, the researchers set up climate stations which collected continuous data on air and soil temperature, wind speed and direction, solar radiation, snow depth and precipitation. (Check out the following (you may need to copy and paste into your browser) for an entertaining look at the challenges of doing this research: https://youtu.be/ty6vwio9LvU).

My beautiful picture

A weather station at the Wind River sight. Credit: Sarah Ellison.

They discovered that soil temperatures were consistently warmer in the western part of the range over the course of the season.

EllisonFig2

 

Soil

Temp.

(deg. C)

 

 

Colder soils are often associated with low levels of available nutrients, because bacteria are less active at colder temperatures, and thus less capable of breaking down nutrients into a form that can be taken up by roots.  In 2014, Ellison and her colleagues measured soil nutrient levels at each site and found generally lower levels in the central (Dietrich) and eastern (Wind River) sites.

EllisonFig3

From top: ammonium, nitrate, phosphate and total free primary amine (TFPA – a proxy for amino acids) availability in the soils at the four sites during the 2014 growing season. Error bars are +/- 1 SE.

There were several other important physiological pieces to this puzzle.  Plants in the west grew more quickly than did plants in the east. Rapid growth was associated with greater photosynthetic rates in the western watersheds. The researchers measured needle nutrient concentration and found that it decreased from west to east. Each year, there was a strong correlation between needle nutrient concentration and branch extension (the measure of tree growth), but the correlation with phosphorus was generally stronger than the correlation with nitrogen.

EllisonFig5

Branch extension in relation to needle phosphorus concentration (left graph) and needle nitrogen concentration (right graph) for three years of the study.

Armed with these findings, Ellison and her colleagues decided to experimentally test whether nutrient availability was limiting growth, particularly in the eastern regions of the Brooks Range.  If so, this would support the hypothesis that cold temperatures and the resulting decrease in nutrient availability were primary factors causing divergence across this vast ecosystem. In June, 2015, the researchers fertilized five trees at each site with a mixture of nitrogen, phosphorus, and potassium fertilizer, and left five similar nearby trees as untreated controls. After one year, branch extension was greatly enhanced at the most eastern site, and only slightly (insignificantly) enhanced at the most western site.

EllisonFig7top

EllisonFig7bottom

Mean annual growth (branch extension) before and after fertilization experiment for fertilized trees (gray circles) and control trees (black circles). Bars are +/- 1 SE.  Fertilization occurred in 2015 (indicated by vertical dotted lines).

For many years, forest ecologists have believed that forests in young glacial soils are nitrogen limited.  This study, and a few other recent studies, thrust phosphorus into prominence as a factor that can limit forest productivity.  Over time, as the climate continues to warm, soils in the eastern Brooks Range will enjoy increased microbial activity, and may no longer suffer as much from nutrient limitation.

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The Agashashok mesic treeline sits on a gentle slope above the Agashashok river. Credit Sarah Ellison.

One surprising finding was that mycorrhizal growth on fine roots was more extensive in central and eastern watersheds.  Abundant mycorrhizae were associated with reduced branch extension, suggesting that these mycorrhizae may be parasitic, rather than mutualistic. The researchers are in the process of expanding their study to an even greater spatial extent of 20 sites distributed across the Brooks Range, which will allow them to further explore how general their findings are across this vast biome.

note: the paper that describes this research is from the journal Ecology. The reference is Ellison, S. B. Z.,  Sullivan, P. F.,  Cahoon, S. M. P., and  Hewitt, R. E..  2019.  Poor nutrition as a potential cause of divergent tree growth near the Arctic treeline in northern Alaska. Ecology100( 12):e02878. 10.1002/ecy.2878. 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.

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%).

EschA

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.

EschD

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.

EschB

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).

EschFig1

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?

EschE

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).

EschFig2

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.

VanWykTurkeyMullein

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.

Wykdamagedturkeymullein

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.

WykFig1

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.

WykFig2b

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.

WykFig2A

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.

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.

StantonCanopy

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.

Stantoncrane

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.

Stantonstockings

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.

Stantonfixationlab

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.

StantonFig1A

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.

StantonFig1B

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.

StantonFig2B

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…

DynarskiEquation

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.

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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.

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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.

DynarskiFig3

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.

DynarskiFig4

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

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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.