Introduced quolls quell melomys

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.

Australian eruptions

Red foxes were introduced to Australia in the mid-19th century to provide hunting opportunities for the English colonists.  Since then, the fox population has exploded and spread throughout the continent, creating happy hunters, but probably leading to the decline of many native mammal species.  As a result, conservation ecologists have attempted to reduce the fox population, primarily using a program of poison baits, but also by reintroducing other predators, such as dingos, that might be able to outcompete the foxes. 

A red fox on the hunt

There are many challenges associated with eliminating foxes and restoring endangered native mammal populations.  As it turns out, red foxes are primarily nocturnal so they are not so easy to hunt, and some of their prey have either gone extinct or are reduced to very small remnant populations.  In cases where fox prey have been reduced but not eliminated, conservation ecologists want to understand what the numerical response of a recovering population will look like.  Will the recovering population increase immediately until another factor, such as food availability, becomes limiting, and then level out at a stable equilibrium?  Or might the recovering population show boom-bust dynamics, increase rapidly until it overeats its resources, then decline sharply from food deprivation, which allows food availability to recover, at which point the recovering population may go through another boom phase? If these boom-bust dynamics (also known as eruptive dynamics) are predictable, that knowledge would allow conservation ecologists to know how long they need to monitor a recovering population to establish its long-term trajectory.

Richard Duncan and his colleagues used data from two types of sources.  Most of the data were population abundance time series of at least seven years (mean = 17 years) from 169 populations of 20 native Australian mammalian species that were recovering following fox control programs.  In addition, the researchers compared their Australian data with time series from seven populations of ungulates that were translocated to northern or mountain regions of Canada, Alaska and Europe.

More than half of the populations were either unchanged or continued to decline following fox removal.  Duncan and his colleagues suggest that fox control might have been inadequate in these cases, or that some other factor continued to limit the native mammalian populations. But 46% of the populations did increase following fox control.  Some of these species, for example the brushtail possum, increased to much higher abundance, and then leveled off. 

The brushtail possum in Austin’s Ferry, Tasmania. Credit: J. J. Harrison.
Abundance of the brushtail possum following intensive red fox control that began in 2003 in Boodoree National Park in eastern Australia. The black-dotted, blue-dashed and solid red curves (in this graph and the graph below) were generated by three different models that were fitted to the data. In this case, the blue dashed curve was the best fit.

But most (56%) of the populations that increased following red fox control showed evidence of eruptive dynamics. For example, the long-nosed bandicoot increased sharply following intensive fox control for about two years, but then crashed sharply, approaching pre-removal levels after another three years.

The long-nosed bandicoot at Craters Lake National Park in Queensland, Australia. Credit: Joseph C. Boone.
Abundance of the long-nosed bandicoot following intensive red fox control that began in 2004 in Boodoree National Park in eastern Australia. In this case the solid red curve was the best fit.

Species with higher maximum rates of increase tended to reach their eruptive peak more rapidly.  In addition, larger species, such as the translocated ungulates, took longer to reach their eruptive peaks.

Time until a mammal population reaches its eruptive peak in relation to the maximum annual rate of population growth (top graph), and the mean body mass of each species (bottom graph). The solid line is the best fit generated by the model, while the dashed lines represent 95% confidence intervals. Both axes use logarithmic scales.

These findings demonstrate that it is not sufficient to show that a threatened population is recovering following removal of an invasive species such as the red fox.  It is possible that even with continued fox control, the recovery will be short-lived, only to be followed by a population crash. Density dependent factors – factors that become more important at high population densities – are probably responsible for many of the observed population crashes.  We have already discussed food availability dynamics; other density dependent factors could include predators being attracted to large prey populations, or disease being more easily transmitted when populations reach a certain level. Because they take longer to reach their eruptive peak and then crash, larger species need to be monitored by conservation ecologists for a longer period of time than do smaller species. Conservation managers need to anticipate these eruptive dynamics as they create their species recovery plans following predator removal.

note: the paper that describes this research is from the journal Ecology. The reference is Duncan, R. P.,  Dexter, N.,  Wayne, A., and  Hone, J.  2020.  Eruptive dynamics are common in managed mammal populations. Ecology  101( 12):e03175. 10.1002/ecy.3175  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.

Fragmented ecosystems: where top-down meets bottom-up

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.

Seagrass stimulated by the return of the green turtle

Christopher Columbus’s journal describes how his ships had to plow through masses of sea turtles to reach the shore of Caribbean Islands. Since the 15th century, populations of the green turtle (Chelonia mydas) were nearly extirpated, primarily to feed the expanding human population. Recent conservation programs have led to a partial recovery in the Caribbean, but current green turtle populations are still a small fraction of what they were historically.

The green turtle, Chelonia mydas.

While the green turtle recovery is good news for turtles, it’s not clear how their favorite food in the Caribbean, the seagrass Thalassia testudinum feels about green turtle resurgence.  When green turtle populations were at their lowest, many lush seagrass meadows performed ecosystem services such as sequestering carbon via photosynthesis, stabilizing marine sediment  and providing important nursery habitats for commercial fisheries.  

Alexandra Gulick and her colleagues were inspired by a similar situation that has been occurring in terrestrial ecosystems.  Since around 1960, wildebeest and buffalo populations in the Serengeti have increased sharply – a result of the sharp decline (or possible elimination) of the rinderpest virus, which previously had controlled the abundance of those two large mammals.  The increase in buffalo and wildebeest populations has profoundly affected the distribution, abundance and productivity of grasses and trees, which of course impacts the entire ecosystem.  Gulick wondered whether the return of green turtles was an analogous situation, in which increases in green turtles would dramatically reduce seagrass meadows and alter ecosystem functioning.

Alexandra Gulick assisted the National Park Service and the U.S. Geological Survey with a mark recapture study of juvenile green turtles. Credit: Kristen Hart.

Gulick and her colleagues were looking for evidence of compensatory growth – increased seagrass growth in response to grazing. Green turtles use a cultivation grazing strategy, in which they select and repeatedly crop the same meadows.  Such behavior would make sense if grazed meadows compensated for grazing by producing biomass at a higher rate, or by producing leaves that were more digestible or nutritious.

A sharp boundary between a grazed and ungrazed seagrass meadow. Credit: Alexandra Gulick.

Working at the Buck Island Reef National Monument, off St. Croix, Virgin Islands, the researchers studied both grazed and ungrazed seagrass meadows, in both shallow water (3-4 meters) and deeper water (9-10 meters). They placed 129 turtle-proof exclosures over grazed and ungrazed meadows during August-October 2017 and January-February 2018. After 7-10 days they measured how much growth had occurred in both types of meadows.  

Divers set up an exclosure in a grazed meadow at Buck Island Reef National Monument. Credit: Alexandra Gulick.

The data table below shows some good evidence for compensatory growth in grazed meadows, particularly in shallow water, but also in some of the deep water meadows. Grass blades grew longer and achieved greater surface area in grazed meadows in shallow water, and also in deep water during the winter (their growth rate was slightly greater during the summer as well, but this increase was not statistically significant).  However, the seagrass in grazed meadows added much less biomass (dried weight) per day per m2.

Seagrass growth in grazed and unglazed meadows at different water depths and seasons. Mass is the increase in biomass (dry weight) per m2 per day. Statistically significant differences between grazed and unglazed meadows are boldfaced.

How can a seagrass blade have more surface area but less biomass?  There are at least two answers to this question.  First, seagrass biomass was measured on a per m2 basis, and ungrazed meadows had more blades per m2. Second, while achieving greater surface area, the seagrass blades from grazed meadows were much thinner, so when dried they weighed much less.  This is important, because putting their resources into surface area allows the seagrass blades to achieve a high photosynthetic rate, which should allow them to recover relatively quickly from sea turtle grazing.  The bottom row in the data table above is a measure of production (measured as mass growth) in relation to initial biomass (P:B).  You can see that P:B in deep water is similar in grazed vs, ungrazed meadows, while P:B in shallow meadows is substantially greater in grazed meadows. This indicates that despite continuous cropping by sea turtles, the grazed seagrass can recover quite nicely.

Gulick and her colleagues wanted to know whether the intensity of grazing might affect productivity.  They counted the number of grazed vs. ungrazed shoots, and the length of grazed vs. ungrazed blades for each sample site, and used those data to calculate grazing intensity.  The researchers then generated a model that calculated P:B in relation to grazing intensity.  The model shows that high grazing intensity increased P:B, indicating that grazing is stimulating increased leaf tissue production.

Increase in production (P:B) in relation to grazing intensity. Dashed lines indicate 95% confidence interval of the linear model.

These findings indicate that increased grazing intensity by recovering sea turtle populations is sustainable in Caribbean seagrass meadows, as seagrass growth was still stimulated at relatively high grazing intensities. Many of the meadows had been grazed continuously for at least two years, and still showed no evidence of being overly stressed by the attention that turtles had given them.  Presumably, compensatory growth by seagrass is an adaptation resulting from the co-evolution of seagrass with green turtles and other hungry herbivores. In support of this coevolution scenario, seagrass in grazed areas reduces the height of its flowers and fruits, reducing consumption of these structures by green turtles, and allowing it to achieve reproductive success.  As green turtle populations continue to recover, it is likely that seagrass meadows will be grazed more heavily, but, at least in most cases, will be able to successfully compensate for even greater grazing levels.

note: the paper that describes this research is from the journal Ecology. The reference is Gulick, A. G.,  Johnson, R. A.,  Pollock, C. G.,  Hillis‐Starr, Z.,  Bolten, A. B., and  Bjorndal, K. A..  2020. Recovery of a large herbivore changes regulation of seagrass productivity in a naturally grazed Caribbean ecosystem. Ecology 101( 12):e03180. 10.1002/ecy.3180.  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

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 pines get help

What makes for a successful invasion?  Is it better to invade with a small, fast moving force or a large, but less mobile force?  Should the invaders be capable of operating independently, or should they have partners (or make partnerships easily) with the existing population? Should resources be allocated to defending the individuals that make up the invasion force, or instead be allocated to recruiting large numbers of less-well-defended invaders?  While military strategists are confounded by these questions, pine trees have solved them. The solution is:

Z-score = 23.39 – 0.63(SM)1/2 -3.88(JP)1/2 -1.09(SC)

This equation was derived about 25 years ago by Marcel Rejmánek and David Richardson who wanted to know what plant attributes were associated with whether pine trees invaded new areas successfully.  They contrasted 12 species that had made successful invasions with 12 species who were primarily noninvasive, and derived the z-score as a quantitative measure of what attributes the invasive species shared.  A higher z-score was correlated with higher invasiveness.  Qualitatively, this equation tells us that invasiveness is correlated with small seed mass (SM), a short juvenile period (JP) and a short interval of time between large seed crops (SC). 

Pine seeds vary in size and number across species. Credit: Jaime Moyano.

Shift to the present time (or at least the recent past). Jaime Moyano and his colleagues were puzzling over whether it was better for these invaders to be capable of operating independently, or whether they should depend on partners.  Ecologists had assumed that independence was a good idea for invaders, and had framed an “ideal weed hypothesis” that plant species that depend on mutualisms are less prone to invade.  Common mutualisms for plants include association with pollinators, seed dispersers and fungi (mycorrhizae).

Pinus contorta (lodgepole pine) invades a forest near Christchurch, New Zealand. Credit: Martin Nuñez.

Moyano and his colleagues tested a prediction of the ideal weed hypothesis by going through the literature to see whether pine species seedlings with higher invasiveness are less dependent on mutualisms with ectomycorrhizal fungi (EMF).  EMF are an association between plant roots and fungi in which the fungal hyphae form a sheath around the root’s exterior and suck up nutrients which they may share with the plant. To test this prediction, the researchers compiled a database of 1206 data points in 34 species based on studies where researchers evaluated how pine seedlings grew with and without EMF inoculation. For each study, they calculated an effect size of EMF as equal to the ln(EMFP/EMFA), where EMFP is seedling biomass with EMF present , and EMFA is seedling biomass with EMF absent.  So a higher effect size indicates that EMF improves seedling growth.

All the pieces were together – all that was left was to do the analysis.  The prediction of the ideal weed hypothesis was that the most invasive species – the species with the highest Z-score – would be expected to have the lowest EMF effect size (be less dependent on mutualism).  The researchers discovered…exactly the opposite.  In general, invasive pines depended heavily on EMF mutualisms to aid seedling growth, while non-invasive pines were less likely to benefit from the services of EMF (top graph below).

EMF effect size in relation to invasiveness (Z score) (top graph). EMF effect size in relation to seed mass (bottom graph).

In addition, the researchers discovered that species with smaller seeds benefitted more from EMF (bottom graph above).  Initially, they were puzzled by these findings that conflicted with conventional expectations.  But then it started making sense…

Parental investment theory tells us that parents have a limited amount of resources that they can allocate to their offspring.  Given this limitation, some plant species make a small number of large seeds that are endowed with large stores of nutrients that the baby can use while germinating and a thick seed coat to protect it.  The downside of this approach is that the large seed might not disperse very far from its parent and may get shaded out by it.  Other plant species make large numbers of very small seeds that are very poorly supplied with nutrients.  The upside of this approach is that the seeds can be blown to new locations that might be ripe for germination (pine seeds are equipped with wings that facilitate traveling in the breeze when released).  The downside of this approach is that germinating seeds might run out of nutrients before they establish themselves.  This selects for a strong dependence on quickly establishing mutualisms to facilitate nutrient intake from the environment. All pines trees ultimately establish EMF, but the smaller-seeded most invasive plants benefit more from EMF early in development, and thus can travel long distances and still get enough nutrients to invade new habitats.

Lodgepole pines invade a forest in Patagonia. This species produces numerous tiny seeds and is highly invasive. Credit: Martin Nuñez.

The question then becomes, how generalizable are these results to other species and other types of mutualisms? The pattern of large seeds showing decreasing response to EMF has been found in some plant families but not others. There are not a lot of data on the relationship between plant invasiveness and their dependence on other types of mutualisms such as pollinators and animal seed dispersers. Moyano and his colleagues caution us that many factors are involved in biological invasions, which makes it very difficult to anticipate which species will be successful invaders.  

note: the paper that describes this research is from the journal Ecology. The reference is Moyano, J., M. A. Rodriguez-Cabal, and M. A. Nunez. 2020. Highly invasive tree species are more dependent on mutualisms. Ecology 101(5):e02997. 10.1002/ecy.2997. 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.

Urchins in hot water

The fabled Mediterranean Sea is under stress from overfishing, pollution, rapid warming, and the associated proliferation of invasive species that thrive in the warming waters.  Two species of rabbitfish (Siganus luridus and Siganus rivulatus) crossed the Suez Canal into the Mediterranean Sea in the 20th century, and now make up about 95% of the herbivorous fish in rocky habitats along the Levant Basin off the Israeli coast.  These fish are voracious feeders on macroalgae that live in the Levant, and they have become much more abundant during the past 30 years in association with increased water temperatures of 2-3 degrees C.

luridusRoberto Pillon

The rabbitfish Siganus luridus. Credit: Roberto Pillon at Wikipedia.

While the Levant has been warming and rabbitfish have been proliferating, things have not gone very well for the purple sea urchin Paracentrotus lividus.  Previously, it had been a very important consumer of macroalgae within the Levant, but its population has collapsed within the past decades.  For his Masters program, Erez Yeruham decided to investigate why the sea urchin population collapsed.  Initially, he and his colleagues thought it was likely that sea urchins were competitively excluded by the invasive rabbitfish. These fish overgrazed much of the algal meadows, forming barren grounds along much of the Israeli coastline. However, during the experiments they did to check that out, they noted that sea urchin mortality occurred in two consecutive summers, but not in other seasons. That led them to explore how sea urchin survival was affected by both the impact of warming water and by competition with rabbitfish.

study site

Researchers construct cages to investigate to investigate the causes of sea urchin population collapse.  See description below. Credit Erez Yeruham.

To investigate competitive exclusion of sea urchins by rabbitfish, the researchers bolted 25 metal cages (50 x 50 x 20 cm) to the rocks approximately 9 meters below the surface of the sea. They set up six different treatments: (1) fish only (F), (2) fish and sea urchins (FU), (3) sea urchins only (U), (4) no fish nor sea urchins (N), (5) cage control – a partial cage that allowed access to organisms (CC), and (6) no cage – an open control plot marked with bolts (NC).  For the treatments with sea urchins (FU and U), the researchers introduced five sea urchins into each cage. For the treatments with fish (F and FU), the researchers cut oblong holes in the mesh large enough for rabbitfish to get through. There were five replicates of each experiment in the fall of 2011 and again in the spring of 2012.

Urchins

Metal cage with five sea urchins (upper left corner of cage). Credit: Erez Yeruham.

Yeruham and his colleagues discovered that fish drastically reduced the abundance of soft algae, but that urchins had no discernable effect.  The researchers suggest that sea urchin density in the cages was low enough that even though sea urchins were eating some soft algae, the effects were too small to be detected. Both fish and sea urchins had very little effect on the abundance of calcareous algae (algae with hard crusty surfaces).

Yeruham2

Mean (+ standard error) dry weight (grams) of soft and calcareous algae for the six experimental treatments.

The researchers compared the amount of food in sea urchin guts when they were caged by themselves, or in cages with fish access.  Sea urchins had 40% more food in their guts when fish were excluded (left graph below).  In addition, they had a 30% greater gonado-somatic index (GSI) when fish were excluded (right graph below – the GSI measures the relative size of the gonads – a high GSI indicates good health and high reproductive potential). So when rabbitfish could visit the cages, sea urchins ate much less and suffered poorer health.

Yeruham3

Mean dry organic gut content (left graph) and GSI (right graph) of sea urchins with and without fish.

The results of this experiment show that rabbitfish have strong competitive effects on sea urchin food intake and overall health. But do warmer waters also help to explain the collapse of sea urchin populations in the Levant?  And might thermal stress interact with food limitation to influence sea urchin health?  To answer these questions the researchers used seawater pumped in directly from the sea into tanks that housed eight sea urchins.  Five tanks received ambient temperature seawater, while five other tanks received water that was chilled by 2 deg. C to mimic water temperatures before sea urchin populations collapsed.  Each tank was divided in half by a partition so that four urchins could be fed (algae) three times a week, while the other four urchins were starved.

One important finding is that during the winter, feeding rates were similar when comparing sea urchins in ambient vs. chilled sea water (two left bars below – those differences are not statistically significant).  However, feeding rates plummeted in the summer when water temperatures exceeded 29 deg. C in the ambient-temperature sea water.

Yeruham4a

Mean algal consumption by sea urchins in ambient vs. chilled water during the winter (two left bars) and summer (two right bars).

Respiration rates (measured as oxygen consumption) are a good measure of metabolic performance. Highest respiration rates were measured in the winter with fed sea urchins (ambient was slightly higher than cold) and in the summer with cold fed sea urchins.  Most notably, when sea water temperatures increased above 29 deg. C in the summer, the respiration rates were very low, even in sea urchins that were well-fed.

Yeruham4b

Mean (+ standard error) respiration rate (measured as oxygen uptake) of starved and fed sea urchins in ambient vs. chilled water during the winter and summer.

What emerges from this series of experiments is that sea urchins feed much more poorly and have lower respiration rates at high temperatures, independent of the effects of competition with rabbitfish.  The researchers also found that survival rates were lower at elevated temperatures.  Yeruham and his colleagues conclude that the direct effects of high temperature and the indirect effects of competition with rabbitfish are important factors that together conspired to lead to the collapse of sea urchin populations in the Levant.  They expect that as sea temperatures increase, rabbitfish will become more dominant in other regions that are now a bit cooler than the Levant. As warming continues and competition increases, Yeruham and his colleagues predict that sea urchin populations will collapse in those somewhat cooler ecosystems as well, changing the structure and functioning of coastal ecosystems across the Mediterranean.

note: the paper that describes this research is from the journal Ecology. The reference is Yeruham, E.,  Shpigel, M.,  Abelson, A., and  Rilov, G..  2020.  Ocean warming and tropical invaders erode the performance of a key herbivore. Ecology  101( 2):e02925. 10.1002/ecy.2925. 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

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.

Turkey mullein trichomes gobble up protective pollen

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

VanWykTurkeyMullein

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

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

Wykdamagedturkeymullein

Turkey mullein with herbivore-damaged leaves

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

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

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

WykFig1

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

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

WykFig2b

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

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

WykFig2A

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

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

note: the paper that describes this research is from the journal Ecology. The reference is Van Wyk, J. I.,  Krimmel, B. A.,  Crova, L., and  Pearse, I. S..  2019.  Plants trap pollen to feed predatory arthropods as an indirect resistance against herbivory. Ecology  100( 11):e02867. 10.1002/ecy.2867. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.

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.

pricklypearcawr_2

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

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

isocoma menziesii complex

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

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

IMG_3938

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.

IMG_vaccum

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.

NellFigc

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.

NellFigb

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.