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.

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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).

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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.

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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.

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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%).

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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.

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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.

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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.

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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.

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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.

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.

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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.

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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.

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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.

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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.

NellFiga

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.

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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.

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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.

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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.

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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.

GarciaFig2

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.

GarciaTable1

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).

GarciaFig6

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.

 

 

 

 

 

 

 

 

 

 

 

Gone gorilla

Humans and lowland gorillas (Gorilla gorilla gorilla) share many features, including strong social bonds among members of their group.  Lowland gorillas differ from humans in that one male (the silverback) dominates the group, which is composed of several females and their offspring. Some mature males are unable to attract females and may be consigned to a solitary existence.  The silverback male mates with females in his group, and may allow other females to join.  However, if a female joins a new group with an unweaned child, there is a high probability that the silverback will kill the child, as a way of getting the female into estrous more quickly, so that he can be the father of more future children.

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A group of gorillas ranges over the landscape. Credit: Céline Genton CNRS/University of Rennes

The Odzala-Kokoua National Park in the Republic of Congo is home to several thousand lowland gorillas. Nelly Ménard and Pascaline Le Gouar (in affiliation with the ECOBIO laboratory CNRS/University of Rennes) have been studying two populations of these gorillas for over 20 years, and have identified and collected long-term data on 593 individuals from the two populations in their study. Working with their student, Alice Baudouin, and several other researchers, they documented that about 22% of the individuals were suffering from a yaws-like disease – an infectious skin disease caused by the bacterium Treponema pallidum pertenue.

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A mother carries her infected infant. Credit: Ludovic Bouquier CNRS/University of Rennes

Females may disperse from their social group several times over the course of their lifetime.  Factors influencing the decision to disperse include availability of a higher quality silverback, reduction of predation, and avoiding inbreeding, resource competition and disease.  Given the prevalence and conspicuousness of yaws, the researchers suspected that these highly intelligent animals would use a variety of cues to inform them of whether they should disperse and which group they should attempt to join.  They expected that females should leave diseased silverbacks for healthy ones, that they should leave groups with numerous diseased individuals and immigrate into groups with healthy individuals, and that diseased females would be less likely to leave their group. Other factors influencing a gorilla’s decision might include group size, group age and whether she had an unweaned infant in her care.

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Silverback gorilla viewed from the mirador (observation post). Credit: Céline Genton CNRS/University of Rennes.

Because they considered so many variables, the researchers used their dataset to construct models of the probability of emigration (leaving the group) and immigration (entering a new group).  The research team categorized each breeding group based on the age of the oldest offspring: young (oldest offspring less than 4 years), juvenile (<7.5 years), mature (<11 years) and senescent (< 14 years). Female gorillas were more likely to emigrate if their group had numerous infected individuals (graph a below) and if the silverback was severely infected (graph b). They were also more likely to leave an older breeding group, perhaps understanding that the silverback would be losing effectiveness in the near future (graph c).  Lastly, females with unweaned infants were very unlikely to leave a group (graph d), presumably unwilling to accept the risk that their infant might starve or be killed if they attempted to join a new group.

GorillaFig2

Probability an adult female emigrates from her group in relation to (a) number of severely diseased individuals within her group, (b) presence of severe lesions on the silverback, (c) age of the breeding group, and (d) presence of an unweaned infant.  Dotted lines (in graph a) and bars (in graphs b, c and d) indicate 95% confidence intervals.

The research team did a similar analysis of factors associated with female gorillas immigrating into a new breeding group.

GorillaFig3

Probability an adult female immigrates into a group in relation to (a) age of group, (b) presence of severely diseased individuals, and (c) group size. Bars (in graph a and b) and dotted lines (graph c) indicate 95% confidence intervals.

 

They discovered that females were much more likely to join younger groups which had younger silverbacks (graph a).  In addition, females tended to join groups without any severely diseased individuals (graph b).  They were also attracted to smaller groups (graph c).

Based on these data, it is clear that disease strongly influences female dispersal decisions.  Females were much more likely to disperse from breeding groups with numerous infected individuals, and strongly avoided groups with more than two diseased individuals. This is not surprising, given how conspicuous these skin lesions are, particularly in the facial regions.  Contrary to expectation, female disease status (infected or not) did not influence female dispersal tendency. The researchers suggest that dispersal might not be particularly costly to the female (assuming she does not have an unweaned infant) because the home range of social groups overlap broadly so it is easy to move from one group to another, and food is also plentiful throughout the range.

Many features of a gorilla’s social environment influence its dispersal decisions. Because diseased females are as likely to disperse as healthy females, the disease pathogen may be more easily spread into previously uninfected gorilla populations.  On the other hand,  dispersing female avoidance of diseased populations has the effect of quarantining the diseased populations. The researchers hope to get a better understanding of the mechanisms of female appraisal of their social environment, so they can predict changes in the prevalence of this pathogen.

note: the paper that describes this research is from the journal Ecology. The reference is Baudouin, A., S. Gatti, F. Levrero, C. Genton, R. H. Cristescu, V. Billy, P. Motsch, J.-S. Pierre, P. Le Gouar, and N. Ménard. 2019. Disease avoidance, and breeding group age and size condition the dispersal patterns of western lowland gorilla females. Ecology 100(9): e02786. 10.1002/ecy.2786.  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.

It’s all happening at the ecotone

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

winsteinatecotone.png

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

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

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

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

Microphallus

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

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

Fig1BCWeinstein

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

 

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

 

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

 

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

Fig3Weinstein

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

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

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

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