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.

Forest Physiognomy

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:

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

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.

Invading hippos

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.


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.


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.


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.


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.


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.


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.

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.


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).


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.


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.


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.


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.


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.


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.


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).


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.


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.


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.


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

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

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

note: the paper that describes this research is from the journal Ecology. The reference is Lamb, R. W.,  Smith, F., and  Witman, J. D..  2020.  Consumer mobility predicts impacts of herbivory across an environmental stress gradient. Ecology  101( 1):e02910. 10.1002/ecy.2910. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2020 by the Ecological Society of America. All rights reserved.

Hot invaders thwart endemic New Zealanders

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


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

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


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

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


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

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


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

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


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

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

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

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


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

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

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

note: the paper that describes this research is from the journal Ecology. The reference is Giejsztowt, J.,  Classen, A. T., and  Deslippe, J. R..  2020.  Climate change and invasion may synergistically affect native plant reproduction. Ecology  101( 1):e02913. 10.1002/ecy.2913. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2020 by the Ecological Society of America. All rights reserved.