Category Archives: Communities and ecosystems

The buzz on trophic cascades

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Herbivores, by their nature, damage plants in natural ecosystems and in agricultural systems.  And predators, by their nature, do a lot of damage to herbivores, either by eating them, or by harassing them in ways that cause them to change their behavior, or in some cases change their morphology or physiology (these are called nonconsumptive effects).  The indirect effect of a trophic cascade in which predators damage herbivores which damage plants, is that predators can benefit plants by their detrimental effect on herbivores.

Much of the research on nonconsumptive effects has focused on aquatic systems because the predator cues are easy to manipulate in the laboratory.  Simply let a predator hang out in a water tank for a while, and then add the predator tank water to a tank with a possible prey item, and study the prey’s response. But there has been little work on nonconsumptive effects in terrestrial systems.  While there has been some research on how auditory cues emitted by terrestrial predators affect vertebrate herbivores, there has been almost no work on how auditory cues affect invertebrate herbivores.  This is surprising, because invertebrates cause enormous damage to agricultural systems. Evan Preisser and his students wondered whether the beet armyworm caterpillar, Spodoptera exigua, a voracious herbivore on many commercially important crops, responded to buzzing emitted by an important predator, the caterpillar-hunting paper wasp (Mischocyttarus sp.). More important, they tested whether the response was substantial enough to have an impact on caterpillar mortality, and subsequent plant development.

Four Spodoptera caterpillars chomp on a soybean leaf. Credit: Michasia Dowdy, University of Georgia, Bugwood.org

Perhaps the biggest challenge was technical.  The researchers needed to come up with a mechanism for delivering an auditory cue to one group of caterpillars that would not be detected by any other nearby group.  They tried various conformations, including separating the cages with soundproofing foam, which, unfortunately, was not soundproof to wasp buzzes.

One of the failed attempts at auditory isolation. Unfortunately, the auditory stimulus was detectable up to two boxes away from the source. Credit: Zachary Lee.

Nothing worked until one of the students suggested using boxes that dry ice was shipped in, reasoning correctly that it should have good insulating properties.  The decibel meter failed to detect any sound from adjacent boxes.

This worked! Credit: Zachary Lee.

Having solved the soundproofing problem, the researchers raised 36 groups of five caterpillars in small cups filled with 25 grams of caterpillar diet. Each cup was placed in a box and subjected to one of three treatments: no-sound control, recorded buzzing of a non-predatory mosquito, or recorded buzzing of a predatory wasp.  The volume was the same for both sound treatments. Each tape went for 12 hours per day, with 2 seconds on, followed by 6 seconds off.  The researchers found that survival was substantially lower for caterpillars that received the wasp treatment (top graph below).  Also, caterpillars that survived the wasp treatment took, on average, longer to develop (bottom graph below), though that difference was not statistically significant.

Survival (top graph ), weight (middle) and time to pupation (bottom) of Spodoptera caterpillars subjected to no sound (green bar), mosquito buzz (yellow) and wasp buzz (red). Different letters above bars indicated statistically significant differences between treatments.

Preisser’s graduate student, Zachary Lee, took the lead in organizing the field experiment.  The researchers wanted to know whether the negative effect of wasp buzzes that they detected in the laboratory had real consequences for agricultural systems.  They surrounded each tomato plant (72  in all) with a mesh bag (to keep the caterpillars in and other insects out), and placed an average of 96 newborn caterpillars on each plant.  Each group of four plants surrounded a speaker that emitted either no sound (control), mosquito buzzing, or wasp buzzing, which were broadcast at levels that caterpillars would experience when an insect was 5 cm away from them.  Each sound was played in a loop of 1 minute on, followed by 10 minutes off, for 12 hours per day.  Lee and his colleagues let the experiment run for 3 weeks, by which time all caterpillars had either pupated or died. They harvested each plant, and calculated the percentage of leaves that were damaged by caterpillars.  Then they dried each plant, including the roots, and weighed them.

Field experiment with four tomato plants positioned equidistant from one central speaker. Each group of four received one of the experimental treatments. Credit: Zachary Lee.

Plant leaves associated with wasp buzzing received the least damage, leaves on control plants received the most damage, and leaves on plants with mosquito buzzing received intermediate damage. Aboveground mass was greater in wasp treated plants than in controls, so the sound of wasp buzzing helps to protect the tomato plants against voracious caterpillar herbivores.

Indirect effects of no sound (green bar), mosquito buzz (yellow) and wasp buzz (red) on tomato plants, via the effects of these treatments on Spodoptera herbivory. Different letters above bars indicated statistically significant differences between treatments.

The researchers did not study caterpillar behavioral changes because these caterpillars are easily disturbed, either freezing or dropping off of plants when approached.  Lee and his colleagues point out that we know very little about how invertebrates, in general, respond to sound cues, as their survey of the literature on prey response to sound cues showed that 181/183 experiments used vertebrate prey.  Given how widespread invertebrates are in agricultural systems, and in ecosystems in general, we need more studies to get a better handle on how invertebrates respond to sound, and most important, how their response influences agricultural systems and ecosystem structure and functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Lee, Z.A., Cohen, C.B., Baranowski, A.K., Berry, K.N., McGuire, M.R., Pelletier, T.S., Peck, B.P., Blundell, J.J. and Preisser, E.L., 2023. Auditory predator cues decrease herbivore survival and plant damage. Ecology, p.e4007. https://doi.org/10.1002/ecy.4007. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2023 by the Ecological Society of America. All rights reserved.

Bat benefits

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Chiroptophobia, the fear of bats, is widespread throughout the world, but also subject to the cultural biases of different regions.  In Europe, bats were historically associated with the Devil, evil spirits and witchcraft. Dante’s Inferno describes the Devil’s wings as being very much like bat wings in form and texture. Vampirism was well established in Eastern European folklore before Bram Stoker’s depiction of Count Dracula routinely transforming himself into a huge vampire bat. Other regions of the world are historically more nuanced in their perspectives. For example, in Madurai, India, worshippers of the Muni god revere the Indian Flying Fox, Pteropus medius, and protect bat colonies from harm.  In Pudukkottai, Pteropus bats are guardians of sacred groves, while in Bihar these same bats bring wealth. But in the Punjab region of India magicians use bat blood to do malevolent magic, and across the border in some regions of Pakistan, bats are associated with evil witchcraft. This is only the tip of the humans/bats cultural iceberg.  For a thorough consideration, you should go to https://www.intechopen.com/chapters/80107.

A vampire bat flies through the night. Credit: Uwe Schmidt, CC BY-SA 4.0 <https://creativecommons.org/licenses

Can ecologists help us resolve this conundrum? The answer is also nuanced.  On the negative side, bats live in dense colonies, are very social and relatively long-lived.  Taken together, these traits allow them to harbor many pathogens, including rabies and coronaviruses, which may be passed on to humans.  On the positive side, bats consume many insects including those that carry diseases.  Recent research has also shown that bats consume insects that eat crops.  Thus, in agricultural ecosystems, there exists a trophic cascade in which bats reduce insect abundance, which leads to an increase in crop production.  Armed with this knowledge, and a recent finding by Tim Divoll that some bats eat insects that defoliate oak and hickory trees, Elizabeth Beilke and Joy O’Keefe decided to explore how important bats were in forested ecosystems.  Does a similar trophic cascade exist, in which bats reduce herbivorous insect abundance, which leads to an increase in tree production?

Underside of oak leaf showing caterpillars hard at work. Credit: Lis Kernan.

To explore the trophic cascade hypothesis, Beilke and O’Keefe set up a three-year experiment (during 2018 – 2020) in the Yellowwood State Forest in Indiana, USA. They built 6 X 7 X 7 meter exclosures that were covered with nylon-mesh netting large enough to allow most insects but small enough to exclude bats. 

Researchers set up a bat exclosure in the forest. A series of ropes and pulleys allowed them to raise the netting each evening and take it down in the morning. Credit: Elizabeth Beilke.

Each experimental unit was a control exclosure without netting, and an experimental exclosure in which the netting was raised during the night to exclude bats, and lowered during the day so that birds could forage.  This allowed the researchers to attribute any treatment effects exclusively to nocturnal animals – basically bats.  They set up seven pairs of exclosures each year; unfortunately one exclosure was destroyed when three trees fell on it during a violent storm. Within each exclosure Beilke and O’Keefe monitored 9 or 10 oak and hickory seedlings during the treatment period.  They counted the number of insects on oak and hickory leaves in May, when the enclosures were set up, and August, when they were taken down.

Basic experimental design. Control plots allowed both bats and birds, while experimental plots allowed birds but excluded bats.

Did bat exclusion increase insect density?  The answer is a resounding “yes” with bat exclusion associated with a 300% increase in insect density in comparison to control plots.

Mean number of insects (+95% confidence intervals) per seedling at the beginning of the field season (left Figure a) and at the end of the field season (right Figure B). Gray dots represent data generated by a statistical model.

Most important, did this increase in insect density lead to greater defoliation of the trees?  Beilke and O’Keefe found that both oaks and hickories suffered greater defoliation when bats were excluded.  The impact on oaks was substantially greater than the impact on  hickories. 

(Figure a – left) Mean defoliation when bats were permitted (top) and excluded (bottom). (Figure b – middle) Mean (+95% Confidence interval) defoliation when bats were permitted (control) or excluded from oak trees. (Figure c – right) Mean (+95% Confidence interval) defoliation when bats were permitted (control) or excluded from hickory trees.

There is some evidence that bats tend to eat more insects that feed on oak trees than insects that feed on hickories. For example, the most common bat in the forest, the eastern red bat, consumed three times more oak-defoliating than hickory-defoliating insect species. Thus bats could be affecting forest composition by preferentially protecting oaks over hickories.  However, given recent declines in bat abundance from white-nose fungus and habitat destruction by humans, losing this protection may be contributing to oak declines in the Eastern United States.

Beilke and O’Keefe point out that bats can negatively influence herbivorous insects directly or indirectly.  Direct effects involve eating herbivorous insects, which are positioned directly on leaves.  Indirect effects can include eating the non-herbivorous adult insects (e.g. butterflies and moths) that produce the herbivorous caterpillars. In addition, some insects are sensitive to the ultrasonic sounds emitted by echolocating bats and may tend to avoid areas populated by bats. Overall, the bat/herbivorous insect/tree trophic cascade results in forests benefitting bats by providing food and places to roost, while bats benefit forested ecosystems by protecting them from herbivory. We now have one more reason to embrace our local bats.

note: the paper that describes this research is from the journal Ecology. The reference is Beilke, E.A. and O’Keefe, J.M., 2023. Bats reduce insect density and defoliation in temperate forests: An exclusion experiment. Ecology, 104(2): e3903. https://doi.org/10.1002/ecy.3903. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2023 by the Ecological Society of America. All rights reserved.

Ants and acacias: friends, foes or frenemies?

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In his massive elegy, “In Memorium A. H. H.”, Alfred, Lord Tennyson laments the death of his friend, Arthur Henry Hallam, at 22 years old. Tennyson writes,

“Who trusted God was love indeed

And love Creation’s final law

Tho’ Nature, red in tooth and claw

With ravine, shriek’d against his creed”

Thus Tennyson accuses the natural world of being rife with strife and violence.

It would be wrong to dispute Tennyson’s complaint outright, but ecologists can present mutualisms, interactions in which both species benefit, as a counterpoint to his argument. One of the best studied is the ant/acacia tree mutualism, in which acacia trees provide food and living accommodations to ants, which protect their home tree against herbivores, including immense creatures such as elephants and giraffes! Previous research had shown that acacias usually grew better if they harbored a colony of protective ants, even though they were providing the ants with costly resources. These resources included swollen thorns (domatia) which ants may use as homes or fungal gardens, and specialized structures (nectaries) which provide ants with sugar.

Swollen thorns (domatia) on an Acacia drepanolobium tree that is hosting Crematogaster nigriceps ants. Credit: Patrick Milligan.

As an undergraduate at the University of Florida, Patrick Mulligan learned about how ecology could be thought of as the study of the economy of nature.  Keeping with the economic metaphor, Mulligan recognized that the tiny ants and relatively large trees trade in the same currency: carbon. He realized that tree growth is simply a measure of how much carbon a tree has to spend on itself. So he asked if ants might be influencing how much carbon is available for both themselves and the tree.

Acacia drepanolobium, the dominant tree in the savanna. Credit Patrick Milligan.

In Laikipia, Kenya, four ant species compete for Acacia drepanolobium host plants, the dominant woody plant in the savanna (see photo above). These ants differ in several traits including how much protection they actually provide, whether they consume tree-produced nectar, how they modify the tree, and how they influence a tree’s water relations (see photo and table below). If a tree can’t get enough water, it is forced to close the stomata on its leaf surface to reduce water loss from transpiration. When stomata are closed, carbon dioxide import is drastically curtailed, and photosynthetic rates (and carbon production) are reduced.

The four ants species studied by Patrick Milligan and his colleagues are Crematogaster sjostedti, C, mimosae, C. nigriceps and Tetraponera penzigi. Credit: Todd Palmer.

To determine how the four ant species influence carbon fixation and water relations in these acacias, Milligan and his colleagues set up a five-year ant-removal experiment between 2013-2018.  They found 48 matched pairs of trees that harbored each ant species (12 pairs of trees per ant species), and then removed all of the ants from one of the two trees by fogging with a short-lived insecticide. The researchers restricted ant recolonization by applying to the base of each tree an annoyingly sticky substance that ants generally avoid. 

After five years (in 2018), Milligan and his colleagues measured photosynthesis and transpiration rates in leaves of each tree, using tools that were specialized for those purposes.  They then extrapolated from these leaf measurements to photosynthetic and water exchange rates for the entire tree crown (where most of the action is). They discovered that trees with C. mimosae (Cm) and T. penzigi (Tp) had substantially higher photosynthetic rates than trees with C. sjostedti(Cs) and C. nigriceps (Cn).  But trees that had their ants removed were statistically indistinguishable in their photosynthetic rates (graph (a) below). In other words, removing ants caused Cm and Tp-trees to reduce their photosynthetic rates, and Cs and Cn tree to increase their photosynthetic rates, so they were equivalent after five years of ant removal.  

(Graph a) Mean (+SE) photosynthetic rate at the tree crown and (Graph b) transpiration rate at the tree crown for acacia trees with ants present or removed. The letters to the side of each data point indicate when two species have statistically significant differences in their value. For example, in graph a, comparing the case where ants were present, the photosynthetic rates for Cm and Tp are not different from each other, but both are significantly greater than the photosynthetic rates for Cn and Cs. However, Cn and Cs have similar photosynthetic rates.

Looking at the table above, you will note that both Cs and Cn do some major alterations to the trees that might compromise carbon production. Though Tp does remove nectaries, it also consumes no nectar, so that interaction may be a wash. Based on these observations, we might suspect that Cs and Cn are actually tree parasites, while while Cm and Tp are closer to true mutualists that actually benefit the host trees. Supporting this idea, removing Cs sharply increased leaf area and also increased water exchange rate (graph (b) above).  And trees that were continuously occupied by Cn also showed reduced leaf area, lower photosynthetic rates (graph a above) and water exchange rates (graph b above) at the tree crown than Cm or Tp. But there is more to the story.

Cn is an aggressive defender against would-be herbivores.  However, it also eats large portions of the tree it inhabits focusing on the nectaries (which produce sugars) and the reproductive structures.  One puzzling consequence of this behavior is that Cn-occupied trees are significantly better than other ant-occupied trees at bringing up subsurface water, perhaps helping the tree to survive droughts.  The researchers plan to measure the root systems of all the trees in hopes of seeing whether Cn-occupation actually alters root development in a way that improves water uptake.

Complicating the story further is a consideration of carbohydrate production. Trees hosting Cs (the stem excavator) had much less starch in their stems than did trees hosting the other species.  Starch is an important source of energy for all plants; in fact trees with Cs removed still had low starch levels after five years.  Presumably the trees that were freed from hosting Cs prioritized growing new branches, or repairing cavities and defending against beetle infestation, over producing more starch for storage. 

Trees occupied by Cm (a nectar consumer) had much higher glucose levels than trees hosting the other three species.  Removing Cm caused the glucose levels to drop sharply (see graph below). Trees hosting the other nectar consumer (Cn) did not show this increase in glucose, possibly because Cn prunes the leaves and eats the flowers, leaving the host tree with insufficient nutrients to increase glucose levels. 

Mean (+SE) glucose levels in the stems of trees hosting each ant species. Notice the sharp drop in glucose concentration five years after Cm removal.

I asked Patrick Milligan how trees get occupied by a particular ant species.  He responded that there are battles for occupancy both between ant species, and sometimes within ant species.  An ant from one colony locks in a death grip with an ant from another colony, they then fall from a branch and kill each other on the ground.  So the bigger colony wins a battle by virtue of having some surviving ants to colonize the tree. One exception is Cs, which has slightly larger and presumably stronger ants, and will sometimes survive a head-to-head battle. Currently, Milligan and his colleagues are investigating how a tree may adjust its leaf physiology when paired with a new ant species, perhaps by activating different genes in response to the novel species.  Though trees cannot choose their ant colonizers, they may be able to adjust to whichever species uses their services.

note: the paper that describes this research is from the journal Ecology. The reference is Milligan, P.D., Martin, T.A., Pringle, E.G., Prior, K.M. and Palmer, T.M., 2023. Symbiotic ant traits produce differential host‐plant carbon and water dynamics in a multi‐species mutualism. Ecology, 104(1), p.e3880. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2023 by the Ecological Society of America. All rights reserved.

Introduced quolls quell melomys

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The cane toad has the distinction of being the world’s largest toad.  It was introduced to Australia in 1935 to control cane beetles that were eating sugarcane (see A toxic brew: toad vs. quoll).  Since their introduction, cane toads have expanded their range by over 2000 km from their release sites, which would be fine if all they did was eat cane beetles.  As it turns out, they are worthless at eating cane beetles, but are very good at being eaten by many predators, including the northern quoll (Dasyurus hallucatus).  This turns out poorly for the quolls, as cane toads are loaded with toxins, which quickly convert a cane-toad-fed quoll into a quoll corpse. Consequently, quoll populations are collapsing across much of Australia.

A northern quoll sports a radio collar. Credit: Chris Jolly

For his PhD work, Chris Jolly was hoping to explore whether he could use behavioral conditioning techniques to train quolls to avoid cane toads before he released them back into the environment.  Unfortunately, while in captivity, the quolls lost their fear of predators, and became easy prey for dingoes, which resulted in a failed reintroduction to Kakadu National Park. In an interesting twist, another graduate student was releasing quolls onto Indian Island for a different purpose, and Jolly decided to regroup and focus his attention on how the prey population responded to a novel predator. In 2017, 54 quolls were released on the northern part of the island, which set up a natural experiment in which quolls were present in the north, and absent in central and southern Indian Island

Ben Phillips and John Moreen release the first batch of northern quolls on Indian Island (Kabarl), Northern Territory, Australia. Credit: Chris Jolly

Working with several researchers, Jolly established four research sites in the north and three in the south.  At each one-hectare site, the researchers set up a 10 X 10 grid of live-traps which they baited with balls of peanut butter, rolled oats and honey (100 traps at each site). The target species was the grain-eating rodent, Melomys burtonia. Over the course of the study, 439 individual melomys were captured, weighed, sexed and implanted with a microchip for identification purposes. The researchers wanted to know how the presence of predaceous quolls influenced melomys abundance, and whether melomys adjusted behaviorally to quoll presence.  

Research sites on Indian Island. Quolls were introduced to the northern part of the island in 2017.

They discovered that the three southern sites (without quolls) maintained relatively steady numbers of melomys throughout the study.  In contrast, the four northern sites (with quolls) showed a sharp decrease in melomys abundance. Complicating the issue, a wildfire broke out in August 2017, affecting only the northern part of the island.  The researchers believe this fire did not affect the melomys in any significant way, as wildfires are common in the area, and several previous studies have shown no effect of wildfires on melomys abundance.

Melomys population estimates at three southern sites (left graph) and four northern sites (right graph). The dashed orange line denotes quoll introduction, while the dashed red line indicates the wildfire in 2017. Error bars are 95% confidence intervals.

Shyness can be an adaptive behavior if predators are in your environment.  Jolly and his colleagues wanted to know if there was any difference in the shyness (or conversely – the boldness) of melomys from the north (with quolls) and south (without quolls). They set up arenas that were baited with the aforementioned peanut butter balls, and placed a live-trap with a melomys at the door to the arena.  The researchers then opened up the trap door and recorded whether the melomys entered the arena within 10 minutes. 

Experimental setup testing melomys responses to open-field tests. Credit: Chris Jolly.

After 10 minutes, each melomys was rounded up and placed back in its trap, and a red plastic bowl was put into the arena.  The trap was then reopened and the researchers recorded whether the melomys interacted with the red bowl.

Looking at the left graph, you can see that in 2017, north island melomys were much shyer than melomys from the predator-free south island. But by 2019, this difference was mostly gone.  But when it comes to exploring a novel object (right graph), the northern melomys still retained some of their fear in comparison to southern melomys.

Figure 4

Left graph.Proportion (+ 95% confidence intervals) of melomys that emerged from live traps within 10 minutes in the open-field test. Right graph. Proportion of melomys that interacted with the novel object in the experiment that tested for neophobia (fear of novel objects).

Lastly, Jolly and his colleagues tested the effect of living with quolls on melomys foraging behavior.  At nightfall, the researchers placed one wheat seed at 81 locations in each site. Control (unmanipulated) seeds were set out at 40 locations while seeds that had been stored with quoll fur (and presumably smelled like quoll) were set out at 41 locations. At daybreak, the researchers counted the number of remaining seeds, so they could calculate seed removal. In the first session conducted shortly after quoll release, they found no evidence of discrimination based on predator scent in either melomys population. But over time, the northern melomys began to discriminate based on quoll scent, while southern quolls continued to forage at the same rate on control and quoll-scented seeds.

Figure 5B

Mean seed take bias (the number of scented seeds – the number of control seeds) taken by north and south island melomys. Error bars are 95% confidence intervals.

The researchers conclude that introduction of quolls as a novel predator influenced melomys in two distinct ways.  First, quolls preyed on them and reduced melomys abundance.  But equally important, quolls changed melomys behavior. Soon after quoll introduction, invaded melomys populations were substantially shyer than the non-invaded populations.  But this changed over the next two years, with a reduction in general shyness in the invaded populations, and an increase in predator-scent aversion. In effect, melomys were fine-tuning their behavioral response to quoll invasion.

Unfortunately, the researchers can’t evaluate whether these behavioral changes result from learning, or from natural selection.  Melomys has a short generation time, so natural selection could be strong, even over a short timespan.  Unfortunately, because of low survival from one year to the next, there were not enough melomys to test for whether individual behavior changed over time as a result of learning.  It is certainly plausible that natural selection and learning operate together to change melomys behavior following quoll introduction.  

note: the paper that describes this research is from the journal Ecology. The reference is Jolly, C. J., A. S. Smart, J. Moreen, J. K. Webb, G. R. Gillespie, and B. L. Phillips. 2021. Trophic cascade driven by behavioral fine-tuning as naıve prey rapidly adjust to a novel predator. Ecology 102(7): e03363. 10.1002/ecy.3363. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2021 by the Ecological Society of America. All rights reserved.

Bird-friendly viticulture

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If you are into wine, the Matorral of central Chile is viticulture heaven. This Mediterranean biome has very warm and dry summers and moderate, rainy winters – ideal conditions for grapes. The Matorral’s natural vegetation is a diverse sclerophyll forest composed of trees and shrubs with hard, short and often spikey leaves. Many of these trees and shrubs are endemic – found in the matorral and nowhere else, as are some of the animals that depend on the vegetation for sustenance, making this region a “biodiversity hotspot”.  Humans enjoy its benign climate as well, which is why most of Chile’s population and largest cities occupy this bioregion.  

Mattoral ecosystem dominates central Chile. Credit: A. Muñoz-Sáez

Unfortunately, the demands of humans for wine and domiciles can come into conflict with the Matorral’s biological diversity.  Much of the natural vegetation has already been cleared and most is privately owned, so there is little potential for setting up large preserves.  As a long-time bird enthusiast, Andrés Muñoz-Sáez wondered whether even small pockets of natural vegetation could help maintain the biologically diverse bird community in the region.  So he and his colleagues conducted a series of systematic surveys to see whether the presence of remnant natural vegetation in the immediate area, or the presence of a continuous forest nearby, increased bird diversity within a vineyard.

A vineyard in central Chile shrouded by fog and surrounded by a sclerophyll forest. Credit: A. Muñoz-Sáez

The researchers conducted 6 auditory and visual surveys for birds in 2014 at 20 vineyards that differed in the amount of surrounding natural vegetation.  They repeated this process early and late in the 2015 breeding season, for a total of 360 surveys. There were three types of surveys: (1) Within the vineyard with no natural vegetation remnants within 250 meters, (2) within remnants within the vineyard, and (3) within native vegetation adjacent to the vineyard.  The mean size of a remnant was 0.17 hectares. All told, the researchers recorded 5068 birds belonging to 48 species.

A burrowing owl keeps watch while perched on a vineyard fencepost. Credit: A. Muñoz-Sáez

Both species richness (left graph below) and overall bird abundance (right graph below) were lowest in the vineyards without remnants nearby, and highest in remnants and in the surrounding matorral. Richness and abundance were very similar in remnants compared to the surrounding matorral. 

Species richness (mean number of species – left graph) and mean number of birds (right graph) per survey conducted in surrounding matorral (M), remnants within a vineyard (R) and in vineyard with no nearby remnants (V). Error bars are 1 standard error. Horizontal bars with *s above bars indicate statistical differences between treatments. * = P < 0.05. *** = P < 0.001.

From the standpoint of species composition (which species were present), bird communities in vineyards with remnants were more like those found in surrounding matorral than like those in vineyards without remnants. Perhaps most important from the standpoint of conserving biological diversity, the mean number of endemic bird species was greatest in matorral (3.02 endemic birds per survey), intermediate within remnants (1.11) and negligible within the vineyard without remnants nearby (0.03).

Muñoz-Sáez and his colleagues advocate retaining remnant native vegetation within vineyards to provide local habitat for native birds.  Their surveys indicated that insectivorous birds were more than six times as likely in remnants than in vineyards far removed from remnants.  From the standpoint of providing ecosystem services to humans, insectivorous birds can benefit vineyard production by removing unwanted insect pests. Given that many remnants are in less productive areas such as steep slopes, or along streams, the costs of maintaining and not developing these remnants are relatively minor, while the benefits to the viticulturist and the ecosystem can be substantial.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Muñoz‐Sáez, A., Kitzes, J. and Merenlender, A.M., 2021. Bird‐friendly wine country through diversified vineyards. Conservation Biology, 35(1), pp.274-284. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2021 by the Society for Conservation Biology. All rights reserved.

Fragmented ecosystems: where top-down meets bottom-up

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Biological diversity is one part of “ecosystem structure”.  Other components of ecosystem structure include which species are present, how abundant they are, whether some species are particularly important for the ecosystem to function, and how all the species interact with each other and the environment.  So ecosystem structure is a pretty loaded concept, and figuring out what controls ecosystem structure has captured the intellect and imagination of many ecologists for a long time.  

Two mutually non-exclusive theories have emerged in discussion of control of ecosystem structure.  The bottom-up control hypothesis argues that the producers (primarily plants) are key, so factors influencing plants (such as sun, water and soils), are paramount for understanding ecosystem structure.  The top-down control hypothesis argues that carnivores eat herbivores and herbivores eat plants, so we should focus our attention on the carnivores who directly influence herbivore abundance, and indirectly (by virtue of their effects on herbivores) influence plant abundance and diversity. 

Rong Wang, his research advisor Xiao-Yong Chen, and several other researchers recognized that Thousand Island Lake would be a perfect place to explore these hypotheses about control of ecosystem structure. Construction of the Xin’an River Dam in 1959 created the lake of 573 km2 that is dotted with more than 1000 islands of varying size.  This creates a natural laboratory for ecologists interested in understanding how island size influences ecosystem structure and specifically to explore the relative importance of bottom-up vs. top-down effects.  In addition, these islands are actually forest fragments surrounded by a matrix that is inhospitable to terrestrial species.  Ecologists are very interested in how fragmentation influences ecosystem structure, because development projects (residential, commercial, public works, etc.) invariably produce fragments of habitat of varying size. Lastly, when establishing nature preserves or conservancies, conservation ecologists need to know how large their reserves should be in order to optimize biological diversity and ecosystem functioning.

The Thousand Island Lake showing a few of its thousand+ islands. Credit: Xiao-Yong Chen.

The major producer in this ecosystem is the evergreen tree, Castanopsis sclerophylla. 

Two Castanopsis sclerophylla trees. Credit: Xiao-Yong Chen.

Their seeds are eaten by two species of rodents, which in turn are eaten by carnivores – primarily snakes, cats and weasels. The researchers knew about these interactions before beginning the study, but they wanted to understand precisely how each player affected ecosystem structure, and how the size of the ecosystem influenced these different levels. They also wanted to explore possible bottom-up effects; for example how does environmental quality affect ecosystem structure.

Hypothesized top-down (orange arrows) and bottom up (green arrows) processes within the ecosystem.

For their study, Wang and his colleagues established research sites on habitats of three different size classes: four small islands (0.6 – 3.2 ha), three medium islands (13-51 ha) and six large habitats (three on the only large island of 875 ha and three on the mainland forest).  Initially the researchers conducted surveys of Castanopsis sclerophylla seedling density, rodent density and environmental conditions.  They discovered that seedlings were much more abundant on the mainland and large island (graph a below), while rodents were much more abundant on medium islands (graph b).  However, small islands were more subject to drought due to lower soil moisture content and higher temperatures – a result of greater surface area exposed to the sun along the perimeter of each small island (graph c and d).   Ecologists call this the edge effect. If you refer back to the first photo in this blog, you will note that the small island in the foreground has a great deal of exposed edge.

Over several years, the researchers systematically placed 12,500 seeds of Castanopsis sclerophylla on the surface across all of the sites, and tracked seed predation and seed dispersal.  Seeds on medium islands survived much more poorly than did seeds on the other habitats (top graph below). Wang and his colleagues also planted 2,750 seeds of Castanopsis sclerophylla in transects across all four sites.  In this case seedling emergence and survival was much lower on small islands than any of the other three habitats (bottom graph).

Top Graph. Survival rates of Castanopsis sclerophylla seeds after being moved away by rodents to a new location (left graph) and overall survival rates until the next spring (right graph). Bottom graph. Emergence rate of 2750 planted seeds (bottom left), and survival through summer (middle) and over the following winter (right).

Piecing together these data, we can see both top-down and bottom-up forces influencing ecosystem structure depending on the size of the habitat. On the mainland and on large islands there are several different types of predators which feed on rodents.  But medium and small islands are just too small to support viable populations of predators.  Thus rodents are super-abundant on medium islands, and eat the seeds that are on the surface.  This is an example of top-down effects causing a trophic cascade, with predators eating rodents, which leads to high seed survival on large habitats. However on medium islands,  predators are absent causing rodents to increase sharply and consume most of the seeds.

But bottom-up effects prevail on small islands, which are so small that that they support only a few rodents.  Seeds that are broadcast on the surface survive predation from the small rodent population relatively well, but seeds that are planted have poor survival because of low soil moisture and high temperature (the edge effect).  I asked Chen whether he thought we could generalize that top-down effects might be more important on large scales and bottom-up effects on small scales.  He responded that both types of regulation are likely to be scale-dependent in many different ecosystems, but that species composition and resource availability would determine how top-down vs. bottom-up control ultimately influences ecosystem structure.

note: the paper that describes this research is from the journal Ecology. The reference is Wang, R.,  Zhang, X.,  Shi, Y.‐S.,  Li, Y.‐Y.,  Wu, J.,  He, F., and  Chen, X.‐Y..  2020.  Habitat fragmentation changes top‐down and bottom‐up controls of food webs. Ecology  101( 8):e03062. 10.1002/ecy.3062.  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.

Forest Physiognomy

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I am old enough that I attended school at a time when educators still taught physiognomy to their students. I recall being attracted to the idea that you could predict someone’s character, criminal or violent inclinations, passions and general temperament by the location of bumps or indentations on the head, the shape of the nose, or the forward projection of the jaw. Dampening my enthusiasm, we were taught physiognomy as an example of pseudoscience, and that we should make sure to not embrace ideas simply because they were intuitively attractive. And this letdown came after I had spent several precious moments learning how to pronounce the word.

Two tranquil foreheads. Credit: Giambattista della Porta: De humana physiognomonia libri IIII. From website of the National Library of Medicine: http://www.nlm.nih.gov/exhibition/historicalanatomies/porta_home.html.

Later, I was delighted to learn in my plant communities class in graduate school that forests had physiognomy, and that reputable scientists actually studied it. Forest physiognomy is the general appearance of a forest, including the height, spacing and structural growth forms of its dominant species.  Michelle Spicer described to me that she went to Central America as an engineering undergraduate student, and became enraptured with tropical forests, including their physiognomy.

Tropical forest showing vast collection of lianas and a few epiphytes. Credit: Michelle Spicer.

Spicer switched from engineering to ecology, and as a graduate student realized that nobody had actually rigorously compared tropical and temperate forest physiognomy. Textbooks might talk about the importance of lianas (vines) and epiphytes (plants that grow on other plants and get nutrients from the air, water or debris lodged in their host plants) in tropical forests.  These same texts might also highlight the importance of the herbaceous layer in temperate forests. 

A temperate forest in the Smokey Mountains, USA. Credit: Michelle Spicer.

But there were few organized data to compare forest physiognomy in the two biomes. Spicer, an undergraduate student in her lab (Hannah Mellor), and her advisor (Walter Carson) chose to compare nine temperate forests and nine tropical forests, spreading across the Americas from Brazil to Canada. Each of these forests (studied by other researchers) had detailed downloadable plant species lists, which also included data about their height and reproductive status.  In total, the researchers went through over 100,000 records to create their dataset.

The figure below highlights the plant physiognomy concept. You can see that most of the species in temperate forests are herbs residing primarily in the forest floor layer.  In contrast, tropical forests have a much more even distribution of types of species, and location of growth.

The physiognomy of temperate and tropical forests. Credit: Jackie Spicer.

Quantitatively, 80% of temperate forest plant species are herbs, while only 7% are trees, and there are relatively few lianas and epiphytes.  In contrast, tropical forests boast a much more even distribution of each plant growth form.

Relative species richness of trees, shrubs, lianas, herbs and epiphytes in temperate and tropical forests.

Going along with the growth form distribution finding, most temperate plant species grow on the forest floor, while more tropical species are actually higher up (upshifted) in the understory – in part due to the prevalence of lianas and epiphytes in the understory layer.

Relative species richness of plants at different layers of temperate and tropical forests.

Spicer and her colleagues caution us that the up-shift in the tropical forest profile may be understated by the data, because even the best inventories are likely to miss epiphytes growing high in the canopy.

The tropical forest epiphyte Guzmania musaica. Credit: Michelle Spicer.

These findings have important implications for conservation and forest management.  Logging of tropical forests removes trees, but also removes lianas and epiphytes associated with trees. Lianas recover well from disturbance, but epiphytes take a long time to return following disturbance. Thus even relatively small-scale logging will significantly reduce biological diversity, not only in the plant communities, but in the many species of animals, fungi and microorganisms that interact with these plants. In contrast, temperate forests may be more resilient to logging, because the diverse herbaceous community can recover quickly, particularly if some canopy cover remains after logging.  Spicer and her colleagues argue that over-browsing by large ungulates, and changes in herbaceous species composition resulting from years of fire suppression are the two primary threats to the extensive biological diversity in the temperate forest herbaceous layer. With many species missing from the herbaceous plant community from these two sources, invasive species can take over, changing forest ecosystem functioning.  The researchers suggest that forest managers should prioritize managing the vast diversity of plant species that inhabit the temperate forest floor and understory.

note: the paper that describes this research is from the journal Ecology. The reference is Spicer, M. E., H. Mellor, and W. P. Carson. 2020. Seeing beyond the trees: a comparison of tropical and temperate plant growth-forms and their vertical distribution. Ecology 101(4):e02974. 10.1002/ecy. 2974.  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.

Tasty truffles tempt mammalian dispersers

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The first humans known to eat truffles were the Amorites (Old Testament victims of Joshua during his Canaan conquest) over 4000 years ago.  Many other animals eat truffles as well; in fact humans commonly use dogs (and sometimes pigs) to help them locate truffles, making good use of their highly developed sense of smell. Apparently pigs and perhaps dogs as well, need to be muzzled so that they don’t consume this delightful fungal delicacy following a successful search.

Ryan Stephens was studying the small mammal community in the White Mountains of New Hampshire as part of his doctoral dissertation, and was particularly interested in what these mammals were eating.  It turned out that fungi comprised about 15% of the diet of the woodland-jumping mouse, white-footed mouse, deer mouse and eastern chipmunk, and about 60% of the diet of the red-backed vole. So he and his colleagues began surveying truffles in the region, and discovered several new species in the process.  

New Hampshire’s White Mountains. Credit: Ryan Stephens

The Elaphomyces truffles we will discuss today are partners in ectomycorrhizal associations.  The fungal hyphae form a sheath around the roots of (primarily) Eastern hemlock trees providing soil nutrients to the tree in exchange for carbohydrates created by the tree’s photosynthetic processes.  What we call “truffles” are actually the fungal fruiting bodies, or sporocarps, which upon maturing develop massive numbers of spores that must somehow be dispersed.  This is a problem for an organism that is attached to underground tree roots.  The solution that has evolved in truffles is emission of volatile substances that communicate with truffle-loving mammals, informing these mammals where the truffles are, and that they are ripe and available.  Mammals dig the truffles up, eat them, and then defecate the spores in a new location that may be many meters or even kilometers away.  

Sporocarps (fruiting bodies) of the four truffle species used in this research. From left to right: (a) Elaphomyces americanus, (b) E. verruculosus, (c) E. macrosporus, (d) E. bartletti. In each photo one truffle has been cut in half, revealing the spores and the spore-bearing structures.

At the Bartlett Experimental Forest in the White Mountains, Stephens and his colleagues set up 1.1 ha grids at eight forest stands that were rich in Eastern Hemlock. Within each grid, they set up 48 16m2 sampling plots for truffle collection.  They used a short-tined cultivator to dig up all truffles within each plot, counting, drying and weighing each sporocarp, and then analyzing each sporocarp for %N. Using simple arithmetic (and some assumptions), the researchers were able to convert %N to % digestible protein.

Short-tined cultivator in action, uncovering two sporocarps. Credit: Ryan Stephens.

It was impossible to measure the depth of each sporocarp, because raking the soil disturbed it too much for accurate measures.  Instead Stephens and his colleagues took advantage of previous research that discovered that soils dominated by ectomycorrhizal fungi have a specific pattern of how a stable isotope of heavy nitrogen (15N) is distributed in relation to the normal isotope (14N), with higher 15N concentrations the deeper you go. The sporocarps have similar 15N concentrations as the soil around them (actually slightly higher, but in a predictable way), so a researcher can measure the 15N/14N ratio of a sporocarp, and estimate its depth in the soil column.  

Stephens and his colleagues discovered that Elaphomyces verruculosus was, by far, the most abundant truffle (Figure a below).  Sporocarps of the four species occupied very different depths, with some overlap (Figure b).  E. verruculosus and E. macrosporus had more digestible protein than the other two species (Figure c).  Lastly, all species had similar sized sporocarps (Figure d).

Sporocarp (a) abundance, (b) depth in soils, (c) % digestive protein and (d) dry mass across the sampling grids. Thick horizontal line in box plots are median values, box limits are first and third quartiles and notches are the 95% confidence intervals. The vertical lines above and below each box extend to the most distant data point that is within 1.5 times the interquartile range.

If a truffle’s sporocarp is deep below the soil surface, we might expect it to emit a stronger chemical signal than a sporocarp nearer to the surface, so it can attract a mammalian disperser.  Having a fully equipped chemical laboratory allowed the researchers to measure the quantity and type of chemical emitted by each species.  They discovered that E. macrosporus and E. bartletti, the two deepest species had the strongest chemical signals – emitting relatively large quantities of methanol, acetone, ethanol and acetaldehyde.

Field research team of Andrew Uccello, Tyler Remick and Chris Burke – each has handsful of E. verruculosus sporocarps. Credit: Ryan Stephens.

The question then becomes, which truffle species are small mammals most likely to eat?  If they go for the easiest to reach, they should prefer E. americanus.  If they go for the most nutritious, they should prefer E. verruculosus and E. macrosporus.  But if they prefer the ones with the strongest signal, they should focus their attentions on E. macrosporus and E. bartletti.

On the surface you might realize that it is difficult to figure out who is eating what.  This is true. To address this problem, the researchers analyzed the quantity and type of fungal spores defecated by mammals that were captured in live traps within their research grids.  Analysis of the feces indicated a consistent preference among all five species of small mammals for the two truffle species with the strongest signals, even though that resulted in them needing to do a bit of extra digging.  The only exception to that trend was red-backed voles consumed much more E. verruculosus than did the other mammals. Recall that E. verruculosus was one of the most nutritious truffles, and that fungi comprise more than 60% of a red-backed vole’s diet. So it was more important for that species to discriminate based on food quality.

Truffle selection by small mammal community. N. insignia = woodland jumping mouse , P. maniculatus = deer mouse, M. gapperi = red-backed vole, P. leucopus = white-footed mouse, T. striatus = eastern chipmunk. Jacob’s selection index measures consumption relative to the availability of each truffle species, with +1 representing strong preference and -1 representing strong avoidance of a particular truffle species. Error bars represent 95% confidence intervals around the mean.

Why don’t the shallow truffle species emit stronger signals? One possibility is that a shallow truffle with a strong signal might get harvested and eaten before it is fully mature, and does not yet have viable spores. A second possibility is that shallow truffles might rely on soil disturbance or mammal activity (burrowing or just scurrying by) to make its way to the surface.  Upon reaching the surface, its spores can disperse in the wind like the spores of more traditional mushrooms. It requires considerable resources to produce these volatile compounds, so a truffle should only produce them if they are highly beneficial. Thus a stronger, energetically costly signal might not be necessary for the shallowest truffles, and may even be counterproductive.

note: the paper that describes this research is from the journal Ecology. The reference is Stephens, R. B.,  Trowbridge, A. M.,  Ouimette, A. P.,  Knighton, W. B.,  Hobbie, E. A.,  Stoy, P. C., and  Rowe, R. J..  2020.  Signaling from below: rodents select for deeper fruiting truffles with stronger volatile emissions. Ecology  101(3):e02964. 10.1002/ecy.2964. 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.

Invading hippos

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

hippoegrit

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

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

hippograze

A grazing hippo. Credit: J. Shurin

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

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

ShurinSIFigPhyto

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

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

ShurinSIFigoxygen

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

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

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

ShurinFig2

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

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

Shurinfig1

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

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

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

Stress frequency structures communities

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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.

ALE_3

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.

IMG_0465

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.