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.


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.

Drought differentially diminishes ecosystem production

Sometimes, even the most carefully conceived experiment is thrown for a loop by Mother Nature.  Good scientists must embrace the unexpected.  Ellen Esch, David Lipson and Elsa Cleland set out to explore how plant communities responded to high, normal and low rainfall conditions.  The researchers set up rainfall manipulation plots that were covered with a clear plastic roof that would allow most light to pass through, but intercept all of the water.  They then reapplied the intercepted water, with each plot receiving either 50%, 100% or 150% of the fallen rain.  The plan was to simulate drought, normal and wet conditions. The natural world had other plans, however, as 2013-2016 were unusually dry years. Fortunately the researchers adjusted, by refocusing their question on how plant communities respond to severe drought  (50% of intercepted rainfall), moderate drought (100%) and normal rainfall (150%).


Herbaceous plant community being irrigated (notice the rainbow). Credit: Ellen Esch.

Esch and her colleagues set up their experiment at the San Diego State University Santa Margarita Ecological Reserve, which has a Mediterranean-type climate with mild, somewhat moist winters and hot dry summers.


Exotic grasses (here showing recently senesced Bromus madritensis) dominated the herbaceous sites. Credit: Ellen Esch

They wanted to know how climatic variability brought about by climate change would influence plant phenology (the timing of periodic ecological events), specifically green-up date (when plants begin turning green) and senescence date (when they turn brown and curtail photosynthesis). They expected that the native species, primarily sage-type shrubs, would be more drought-resistant than the exotic herbaceous vegetation, which was dominated by brome grass.  Climate change is predicted to increase climatic variability, which should increase the frequency and intensity of severe droughts (and also of unusually wet years).

An important measure of ecosystem functioning is its productivity – the amount of carbon taken up by an ecosystem, usually by photosynthesis.  More productive ecosystems have more energy available to feed consumers and decomposers.  More productive ecosystems also take up and store more carbon dioxide from the atmosphere, which can help reduce climate change. The researchers used a reflectance radiometer to calculate the Normalized Difference Vegetation Index (NDVI), which essentially calculates how green an area is, and is a good measure of productivity.  Esch and her colleagues hypothesized that drought would reduce overall ecosystem NDVI, but that native vegetation would be more buffered against the negative effects of drought than would the invasive exotic vegetation.


A student from a plant physiology class at San Diego State University measures NDVI. Credit: David Lipson

Each year from 2013 – 2016, the researchers set up 30 3X3 meter plots; 15 plots were dominated by exotic herbaceous species such as brome, and 15 plots had mostly native shrub species such as sage. Plots were treated the same, except for receiving either 50%, 100% or 150% of the fallen rain, which corresponded to severe drought, moderate drought and normal rainfall, respectively. Periodically, the researchers used a radiometer to measure NDVI for each plot.  They discovered that, as expected, drought reduced NDVI much more in the plots dominated by exotic herbaceous species (top graph below) than in the plots dominated by native shrubs (bottom graph).


NDVI on each measurement date for plots dominated by (top graph) exotic herbaceous species and (bottom graph) native shrub species. Red square = severe drought treatment, green circle = moderate drought, blue triangle = normal precipitation. Error bars = +/- 1 standard error.

What caused this difference in response to drought between exotic plant-dominated and native plant-dominated communities?  Mechanistically, the native shrubs have deeper roots than the exotic grasses, which may allow them to take up more water.  But how does this translate to differences in green-up date and senescence date?


A student measures stem elongation on a senescent native shrub, the black sage Salvia mellifera, near the very end of the growing season. Credit: Ellen Esch.

The researchers used two different NDVI measures to help answer this question.  Maximum NDVI is the greatest daily NDVI measure over the course of the growing season.  It is correlated with the maximum productivity of the plant community (at its greenest!).  In contrast seasonally integrated NDVI is a measure of productivity summed over the entire growing season.  Keeping those distinctions in mind, under extreme drought maximum NDVI was much lower in the exotic plots than the native plots.  But exotic plot performance increased with rainfall, so that under the wettest conditions (normal rainfall), exotic plot maximum NDVI was similar to native plot maximum NDVI (graph a below). However, when considered over the entire growing season, native plots were consistently more productive than exotic plots (graph c below).


Effect of rainfall on (a) maximum NDVI (top left), (c) seasonally integrated NDVI (top right), (b) green-up date (bottom left) and (d) senescence date (bottom right). Colors indicate dominant plot community composition (yellow = herbaceous, green = shrub) and point shape indicates growing season year (circle = 2013, square = 2014, diamond = 2015, triangle = 2016).

Phenology played an important role accounting for these differences in seasonally integrated NDVI.  At all rainfall levels, the native plant communities greened-up well before the exotic plant communities (graph b above). Exotic plants greened-up somewhat earlier as rainfall increased, while native plant green-up date was independent of rainfall. At all rainfall levels, native plots senesced about one month later than exotic plots, with increased rainfall delaying senescence in both native and exotic plant communities (graph d above).

Esch and her colleagues conclude that species composition (native shrub vs. exotic herbaceous plants) and drought both influence phenology and productivity in this important ecosystem. Climate change is predicted to increase the frequency of extreme droughts in this and other ecosystems.  Consequently, drought coupled with invasion by herbaceous species threatens to sharply reduce ecosystem productivity, which will decrease the food available for consumers and decomposers, and simultaneously reduce the amount of carbon dioxide taken up and stored by the ecosystem, thereby contributing to further climate change.

note: the paper that describes this research is from the journal Ecology. The reference is Esch, E. H.,  Lipson, D. A., and  Cleland, E. E.  2019.  Invasion and drought alter phenological sensitivity and synergistically lower ecosystem production. Ecology  100(10):e02802. 10.1002/ecy.2802. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.

Tadpoles shun trout across time

At a young school child (so long ago I can’t recall exactly when) I was exposed to Ernst Haeckel’s dictum that “ontogeny recapitulates phylogeny.”  More interested in language than biology at the time, I thought “cool – three words that I’m clueless about.” Though biological thinking about ontogeny – the processes of growth and development – has changed since Haeckel’s time, interest has, if anything, grown more intense across disciplines. Tiffany Garcia has explored her lifelong fascination with ontogeny by focusing her research on amphibians, which are famous for their distinct stages of development, each with unique habitats and ecological requirements. Working with eggs and tadpoles of the Pacific chorus frog (Pseudacris regilla), Garcia and her colleagues investigated whether stress associated with the presence of predators during one developmental stage (for example an egg) would carry over to influence behavior or development of subsequent stages.

chorus frog

The Pacific chorus frog (Pseudacris regilla). Credit Brett Hanshew.

A tadpole’s anti-predator strategy can be influenced by other factors besides carry-over from earlier developmental stages.  For example, we might expect that tadpoles whose ancestors lived in association with predators for many generations might have evolved a different anti-predator strategy than did tadpoles whose ancestors lived in a less threatening environment (this would be an adaptive effect). Tadpoles may also show very short-term changes in behavior or development (this is termed plasticity) if exposed to a cue that indicated a possible predation threat.


Collecting newly laid eggs at Three Creeks Lake. Credit: Lindsey Thurman

These three processes operate over very different time scales (long term – adaptive; intermediate term – carry-over; short term – plastic).  Garcia and her colleagues designed an experiment to explore how these processes might interact to influence a tadpole’s anti-predator strategy.  To investigate long term adaptive effects, the researchers collected newly laid (fertilized) eggs from lakes with and without rainbow trout (Oncorhynchus mykiss). They investigated carry-over effects by conditioning these eggs with four different environments during development: (1) trout odor, (2) cues from injured tadpoles (alarm cues), (3) trout odor paired with alarm cues, and (4) a water control (no odors nor cues).  The researchers created alarm cues by grinding up four juvenile tadpoles in 150 ml of water, and trout odor by housing 30 juvenile rainbow trout in a 200 L tank filled with well water.  They then conducted behavioral and developmental assays on tadpoles to see how adaptive, carry-over and plastic effects influenced tadpole growth, development and behavior.


Overview of the experimental design.

Garcia and her colleagues discovered that early exposure to trout odor had very little effect on growth and development, with body size and stage of development equivalent to that of controls.  In contrast exposure of eggs to tadpole alarm cues or to alarm cues + trout odor resulted in smaller, less developed fish (see table below).  In addition there was no effect of evolutionary history – eggs from lakes with and without trout showed similar patterns of growth and development.


Tadpole size and development in response to the four conditioning  treatments.  Higher Gosner stage numbers indicated more developed tadpoles. A tadpole hatches at Gosner stage 21 and begins metamorphosis at Gosner stage 42.

The next question is how do tadpoles respond behaviorally from exposure to different environments over the long, intermediate and short time scale?  To test tadpole anti-predator behavior, the researchers placed an individual tadpole into a tub that had a 6 X 8 cm piece of corrugated black plastic, which the tadpole could use as a refuge.  The researchers added to each tub one of the following: water (as a control (C)), tadpole alarm cues (AC), trout odor (TO), or alarm cues + trout odor (AC+TO).  After an acclimation period, a researcher noted the position of the tadpole (under the refuge or out in the open) every 20 minutes over a 3-hour time period.

There were no effects of evolutionary history on refuge use.  Tadpoles from lakes with and without trout showed similar patterns of refuge use.  However, embryonic conditioning to alarm cues and trout odor had a large effect on refuge use.  The left graph below shows the response of tadpoles from all four conditioning groups (C, AC, TO and TO+AC) to the addition of water.  As you can see, tadpoles that hatched from eggs that were conditioned with AC+TO were most likely to use refuges, while tadpoles from AC only or TO only eggs were somewhat more likely to use refuges. The pattern repeats itself when tadpole alarm cues are added to the water (second graph from left).  However when trout odor is added to the water, the responses are much more extreme, but follow the same pattern (third graph).  Lastly, when confronted with alarm cues and trout odor, tadpoles increase refuge use dramatically, but again show the same pattern, with tadpoles from control eggs using refuges the least, and tadpoles from eggs conditioned with alarm cues and trout odor using refuges the most (right graph).


Refuge use by tadpoles in response to embryonic conditioning and experimental exposure. C = water control, AC = tadpole alarm cue, TO = trout odor, and AC+TO = tadpole alarm cue and trout odor. Blue bars are means and gray bars are 95% confidence intervals.

There are two processes going on here.  First, over the short term, tadpoles are more responsive to the strongest cues, increasing refuge use when exposed to both tadpole alarm cues and trout odor.  Second, over the intermediate term, there is solid evidence for carry over effects.  Tadpoles that hatched from eggs conditioned with alarm cues and/or trout odor showed markedly increased refuge use than did tadpoles that hatched from control eggs.

These predator-induced responses impose a cost to the tadpoles.  Tadpoles exposed to alarm cues and trout odor while still in the egg were smaller and less developed, and probably metamorphosed into smaller frogs.  Many studies have shown that smaller frogs have reduced reproductive success.  The researchers recommend further studies to explore these trade-offs between survivorship, growth rate, development rate and size at metamorphosis. These studies are particularly essential, because rainbow trout are a non-native predator to these lakes.  Studies such as these allow conservation ecologists to understand the evolution and development of predator-prey interactions when novel species are introduced into an ecosystem.

note: the paper that describes this research is from the journal Ecology. The reference is Garcia, T. S.,  Bredeweg, E. M.,  Urbina, J., and  Ferrari, M. C. O..  2019.  Evaluating adaptive, carry‐over, and plastic antipredator responses across a temporal gradient in Pacific chorus frogs. Ecology  100( 11):e02825. 10.1002/ecy.2825.  Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.












Fast living vs. slow and steady

Fast living makes headlines, as evidenced by such notables as Freddie Mercury, Paul Walker and Lamar Odom.  Unfortunately the first two are dead while Odom was narrowly brought back from a near-death experience – all were victims of their fast life styles.  Like humans, some birds live fast and die young, while others live slow, but may survive to relatively ripe old ages.

Pic 2

The tiny rifleman (Acanthisitta chloris), reintroduced in Tiritiri Matangi, New-Zealand.  This endangered bird feeds on insects that it gleans from tree trunks.  It often has two clutches of 2-5 young per year. Credit: Simon Ducatez.

Simon Ducatez studied invasive cane toads with Rick Shine in Australia, and became interested in why some species were more likely than others to successfully invade new habitat.  The problem for answering that question is that most invasions are not studied until after the invasive species becomes established; by that time it may be too late to identify exactly what factors were responsible for the successful invasion. On his first visit to New-Zealand in 2016, Ducatez discovered ecosanctuaries – enclosed wildlife reserves where invasive predators are eliminated, and native animals (mostly birds) are introduced. He realised that these introductions could provide invaluable information on why species thrive or fail to become established in a new environment. At about the same time, a colleague drew his attention to a database developed by the Lincoln Park Zoo (LPZ) in Chicago, Illinois, which contains data on hundreds of intentional release events (translocation attempts), including information on the survival and reproduction of the released individuals. Analyzing how a species life history could affect the survival and reproduction of these voluntarily introduced populations would provide answers useful for restoration biologists who wish to return native species to habits where they were now extinct, and to ecologists who want to identify the factors promoting biological invasions.

Pic 7

The relatively massive and flightless south island takahe (Porphyrio hochstetteri), reintroduced in New-Zealand.  This bird was thought to be extinct but was rediscovered in 1948 and has benefited from active restoration programs. Credit: Simon Ducatez.

Life history traits are adaptations that influence growth, survivorship and reproduction of individuals of a particular species.  For each species in the LPZ dataset, Ducatez and Shine used the bird literature to gather data on body mass and four life history traits: maximum lifespan, clutch size, number of clutches per year, and age at first reproduction. They then used a statistical procedure – principle components analysis – which described each species based on their life history strategy.  Fast life styles were associated with small bodies, short lifespans, large clutch size and number, and early reproduction.  Slow life styles were associated with large bodies, long lifespans, small clutch size and number, and delayed reproduction. Ducatez and Shine then asked a simple question based on 1249 translocation events in the LPZ dataset – how do fast life style birds perform in comparison to slow life style birds following translocation?

It turns out that slow life style birds are much better at surviving translocation than are fast life style birds, at least when measured in the short term (one week) and the medium term (one month).


Association between life style as measured by principle component analysis (PC1 on X-axis) and survival (proportion of translocated individuals still alive on Y-axis). The left graph is survival to one week, while the right graph is survival to one month. 

In contrast, following translocation fast life style birds are more likely to attempt breeding and successfully breed than are slow life style birds.


Association between life style and probability of attempting breeding (left graph) and successfully breeding (right graph).

Ducatez and Shine suggest that both restoration biologists and invasion ecologists could use these findings to address major questions in their respective fields.  Restoration biologists wishing to return native species to previously occupied habitat might adopt different approaches based on a species life style. Species with fast life styles suffer from low survival, so restoration biologists should focus on promoting survival by controlling predators or provisioning extra food. Species with slow life styles suffer from low reproductive success, so conservation managers might consider providing extra nest boxes or other resources that promote successful breeding.


A successful foraging event for an Atlantic puffin (Fratercula arctica), reintroduced in Maine, USA. Credit: Simon Ducatez.

This research informs invasion ecologists that the same trait can have opposite effects on the likelihood that a biological invasion will actually happen.  Thus a slow life style species is more likely to survive moving to a novel habitat, but is unlikely to breed successfully once it gets there.  In contrast a fast life style species is less likely to survive the move, but if it does survive, it may be more likely to successfully reproduce. How this plays out in actual biological invasions is yet to be determined, but at least we now have a better grasp on what factors we should be examining.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Ducatez, S. and Shine, R. (2019), Life‐history traits and the fate of translocated populations. Conservation Biology, 33: 853-860. doi:10.1111/cobi.13281. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2019 by the Society for Conservation Biology. All rights reserved.

Invasive crayfish hit the self-destruct button

One important feature of a biological invasion is that invaders can change an entire ecosystem in a substantial way.  A possible outcome of this change is that, in theory, an invasive species could inadvertently make an ecosystem less suitable as a habitat for itself.  Does this happen, and if so, under what circumstances?  One reason invasive species are so successful is that they usually can increase in population size very quickly.  Ecologists have discovered that species with the potential to increase very quickly may also have the potential to decline equally rapidly and then increase again, going through repeated boom-bust cycles of population size.  Thus if an invasive species starts to decline, it does not always mean that this decline will continue over time. Consequently, monitoring a biological invasion for only a few years may give a misleading picture of long-term prognosis for the invasive species and the ecosystem.

Eric Larson was able to address these problems when he began his postdoctoral research with David Lodge at the University of Notre Dame in 2014. Lodge (and John Magnuson before him) has studied the rusty crayfish (Faxonius rusticus) invasion in 17 northern Wisconsin lakes since the 1970s, using the same bait (beef liver) and the same traps on the same days each year.


Crysta Gantz prepares to bait a trap with beef liver, which the crayfish love, but she – not so much! Credit: Eric R. Larson.

Three graduate students (the other co-authors of the paper) had continued data collection and done extensive mapping of the lake bottoms.  When Larson joined the research program he had about 40 years of data and 17 well-described lakes.  He knew that rusty crayfish were declining in some lakes and not others, and he and his colleagues were ready to explore whether these declines could be tied in to some environmental variable that the crayfish were influencing in some lakes, but not others.


Allequash Lake. Credit Eric R. Larson

As an avid fisherman (more in my mind than in actuality), I have, on many occasions, caught a nice bass only to have it regurgitate the contents of its stomach, which usually includes bits of crayfish.  As it turns out, predacious fish such as bass love to eat crayfish, and crayfish are more likely to survive in environments that provide hiding places such as rocks or luxurious macroalgae that grow in sand or muck. The problem is that crayfish enjoy dining on macroalgae, so they can do themselves a disservice by eating their shelter from predators, effectively changing their environment so that their invasion is no longer sustainable.  Does this actually happen?


Two rusty crayfish discuss the issues of the day. Credit: Eric R. Larson.

Larson and his colleagues continued collecting data on 17 lakes, and used their long-term data set to evaluate whether rusty crayfish populations were not declining (steady or increasing), declining or occupying an ambiguous gray zone where there was no clear trend in how the population was changing. The analysis showed that three lakes were not declining since the rusty crayfish invasion, eight lakes had declined substantially and six lakes were ambiguous.


The researchers turned their attention to the lake-bottom substrate.  Were rusty crayfish more successful in rocky bottom lakes that gave them continuous predator protection?  Their analysis indicated that the three lakes where the invasion was going strong had the rockiest substrate, while the eight lakes experiencing population declines after the rust crayfish invasion were significantly less rocky.


Proportion rocky substrate in lakes whose rusty crayfish populations are in decline (red), have an ambiguous trend (black) or are not in decline (blue). The horizontal line within each box is the median value, box bottom and top are 25th and 75th percentile, and whiskers are the 10th and 90th percentile. Non-overlapping letters above the bars (a and b) indicate significant differences between the groups.

The researchers conclude that in the absence of rocky substrate, the rusty crayfish is eating the aquatic macrophytes that grow from the sandy lake bottom, thereby exposing itself to predators.  Larson and his colleagues recommend simultaneous surveys of crayfish populations and density of aquatic macrophytes to see whether lakes may oscillate between states dominated by one or the other.


Captured crayfish. Photo Eric R. Larson

Researchers want to know how commonly invasive species modify habitat in a self-destructive way.  A literature review of invasive species declines failed to find much evidence, but there are not enough long-term data sets to get a sense of how frequently this occurs. The problem is that researchers need to monitor the invasive species population and the relevant habitat variables for an extended time period.  The jury is still out on this question and only time (and careful data collection) will tell.

note: the paper that describes this research is from the journal Ecology. The reference is Larson, E. R.,  Kreps, T. A.,  Peters, B.,  Peters, J. A., and  Lodge, D. M.  2019.  Habitat explains patterns of population decline for an invasive crayfish. Ecology  100( 5):e02659. 10.1002/ecy.2659. 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.

Invasive crayfish depress dragonflies and boost mosquitoes

Paradoxically, obliviousness and intense focus can be two sides of the same coin, as the following story highlights.  As a new graduate student at the University of Minnesota, I took a field ecology course at the University’s field station at Lake Itasca (famously known as headwaters of the Mississippi River).  One afternoon we watched dragonflies at a small pond; the male dragonflies were obviously patrolling territories and behaving thuggishly whenever intruders came by, and amorously whenever females of their species approached.  Surprisingly, territorial males chased off male intruders of any species, even though they posed no reproductive threat to them.  Why, I wondered…  So I sat there for many hours and kept very careful track of who chased whom, and for how long.  Big focus time. Ultimately, these observations blossomed into my doctoral dissertation.  Unfortunately, these observations also blossomed into the most virulent case of poison ivy known to humanity, as my intense focus on dragonflies obliviousized me to the luxurious patch of poison ivy, which served as my observation perch.

Anax junius Henry Hartley

Anax junius dragonflies in copula.  The male has the bright blue abdomen.  Credit: Henry Hartley.

Despite this ignoble incident, dragonflies remain one of my favorite animal groups.  They are strikingly beautiful, brilliant flyers, and fun to try to catch. In addition, they have so many wonderful adaptations, including males with penises that are shaped to scoop out sperm (previously introduced by another male) from their mate’s spermatheca, and females who go to extremes to avoid repeated copulation attempts, for example, by playing dead when approached by a male. Thus I was delighted to come across research by Gary Bucciarelli and his colleagues that highlighted the important role dragonflies play in stream ecosystems just west of Los Angeles, California.

Back Camera

Captured dragonfly nymph.  Dragonflies require from one to four years to develop in aquatic systems, before they metamorphose into terrestrial winged adults. As nymphs, they are fearsome predators on aquatic invertebrates. As adults, they specialize on winged insects, though there are stories of them killing small birds. Credit: Gary Bucciarelli

Bucciarelli and his colleagues came up with their research question as a result of working in local streams with students on a different project.  They wanted to know if invasive non-native crayfish (Procambarus clarkii) affect the composition of stream invertebrates and whether removal of crayfish could lead to rapid recovery of these invertebrate communities.

crayfish, egg masses, clutches

Invasive crayfish, P. clarkii, sits on the stream bottom. Credit: Gary Bucciarelli

The researchers collected stream invertebrate samples and noticed a dramatic pattern – in all the streams with crayfish there were numerous mosquito larvae, but in all of the streams without crayfish there were no mosquito larvae and much greater numbers of dragonfly nymphs. This led them to formulate and test two related hypotheses. First, dragonfly nymphs (Aeshnaspecies) are more efficient predators on mosquitoes (Anopheles species) than are the invasive crayfish. Second, crayfish interfere with dragonfly predation on mosquitoes in streams where crayfish and dragonflies are both present.

Field Sampling

Student researchers collect stream samples. Credit: Gary Bucciarelli

Bucciarelli and his colleagues systematically sampled 13 streams monthly from March to October 2016 in the Santa Monica Mountains. Eight streams have had crayfish populations since the 1960s, while four streams never had crayfish, and one stream had crayfish removed as part of a restoration effort in 2015. Overall, streams with crayfish had a much lower number of dragonfly nymphs than did streams without crayfish.  In addition, streams with crayfish had substantial populations of Anopheles mosquitoes, while streams without crayfish (but much higher dragonfly populations) had no Anopheles mosquitoes in the samples.


Number of mosquito larvae (MSQ) and dragonfly nymphs (DF)  by month in streams with crayfish (CF – top row of data) or without crayfish (CF Absent – bottom row)

This field finding supports both of the hypotheses, but the evidence is purely correlational.  So the researchers brought the animals into the laboratory to test predation under more controlled conditions.  They introduced 15 mosquito larvae into tanks, and exposed them to one of four treatments: (1) a single crayfish, (2) a single dragonfly nymph, (3) one crayfish and one dragonfly nymph, or (4) no predators. The researchers counted the numbers of survivors periodically over the three day trials. As the graph below indicates, dragonflies are vastly superior consumers of mosquito larvae compared to crayfish.  However, when forced to share a tank with crayfish, dragonflies stop hunting, either huddling in corners or actually perching on the crayfish.  By 36 hours into the experiment, all of the dragonflies had been eaten by the crayfish.  After three days, mosquito survival was similar when comparing tanks with crayfish alone with tanks that had both a crayfish and a dragonfly.


Mean number of surviving mosquito larvae in tanks with a lone dragonfly (DF), a lone crayfish (CF), one crayfish and one dragonfly (CF+DF) in comparison to controls with no predators.

Bucciarelli and his colleagues conclude that dragonfly nymphs are much more efficient predators of mosquito larvae than are crayfish. But when placed together with crayfish, dragonfly foraging efficiency plummeted. Field surveys showed a negative correlation between crayfish abundance and dragonfly larvae, and much greater mosquito larva populations in streams with crayfish.  This supports the conclusion that invasive crayfish cause mosquito populations to increase sharply by depressing dragonfly populations and foraging efficiency.  This is a complex trophic cascade because crayfish increase mosquito populations despite eating a substantial number of mosquito individuals.

The researchers argue that crayfish probably relegate dragonfly larvae to inferior foraging habitats, thereby limiting their efficiency as mosquito predators. As such, ecosystem services provided by dragonflies to humans are greatly diminished.  Recently, several new mosquito species that are disease vectors have moved into California.  Thus the loss of dragonfly predation services could pose a public health threat to the human population.  Bucciarelli and his colleagues recommend removing the invasive crayfish to restore the natural community of predators, including dragonflies, which will then naturally regulate the increased number of potential disease vectors.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Bucciarelli, G. M., Suh, D. , Lamb, A. D., Roberts, D. , Sharpton, D. , Shaffer, H. B., Fisher, R. N. and Kats, L. B. (2019), Assessing effects of non‐native crayfish on mosquito survival. Conservation Biology, 33: 122-131. doi:10.1111/cobi.13198. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2019 by the Society for Conservation Biology. All rights reserved.

Quoll vs. toad: a toxic brew

A native of Central and South America, the cane toad, Rhinella marina, was introduced to Australia in 1935 with great fanfare. The plan was for the voracious cane toad to eat all of the grey-backed cane beetles that were plaguing sugar cane plantations in northern Australia (a similar introduction had been successful in Puerto Rico).  But the plan failed, in part because there was no cover from predators, so the toads were not enthusiastic about hanging out in sugar cane plantations, and in part because adult beetles live primarily near the tops of sugar cane, and cane toads are poor climbers.


A cane toad. Credit: Ben Philips

So now, northern Australia has a cane toad plague, which is wreaking havoc on ecosystems, and threatening many native species, including the northern quoll, Dasyurus hallucatus. These omnivorous marsupials eat fruit, invertebrates and small vertebrates.  Unfortunately, their long list of food items includes cane toads, which are highly toxic to most consumers, having poison glands that contain bufotoxin, a composite of several very nasty chemicals.  If a northern quoll eats a cane toad, it’s bye bye quoll.

Male captive born northern quoll_EllaKelly

A northern quoll. Credit: Ella Kelly.

Unfortunately most quolls have not gotten the message; huge numbers are dying, and populations are going extinct.  As toads continue their invasion from north to south, more quoll populations, particularly those in northwestern Australia, will be at risk.


Map of Australia showing past (light shading) and recent (dark shading) northern quoll distribution, and present (solid line) and future (dashed line) cane toad distribution.

Some quolls show “toad-smart” behavior and don’t eat toads. Ella Kelly and Ben Phillips are trying to understand how this happens. This is particularly important because a few quoll populations have managed to survive the cane toad plague by virtue of being toad-smart (though 95% of quoll populations have gone extinct in the wake of the cane toad wave). The researchers reason that if there is a genetic basis to toad-smart behavior, it might be possible to introduce toad-smart individuals into populations that have not yet been overrun by cane toads.  These individuals with toad-smart genes would breed and spread their genes through their adopted population.  This strategy of targeted gene flow would give the recipient population the genetic variation needed, so that some individuals (those with toad-smart genes) would be more likely to survive the cane toad invasion.  Over time toad-smart behavior would spread throughout the population via natural selection.

Targeted gene flow requires the trait to be influenced by genes.  To test for a genetic basis to the toad-smart trait, Kelly and Phillips designed a common-garden experiment, capturing some quolls that had survived the cane toad invasion (toad-exposed), and others from regions that had not yet been exposed (toad-naïve).  At Territory Wildlife Park, Northern Territory, Australia, the researchers bred these quolls to create three lines of offspring: Toad-exposed x toad-exposed, toad-exposed x toad-naïve (hybrids), and toad-naïve x toad-naïve.  They raised these three lines under identical conditions at the park. Kelly and Phillips then asked, are there behavioral differences in how these three lines respond to cane toads?


Northern quoll captured in Northern Territory, Australia. Credit: Ella Kelly.

The researchers set up two experiments.  First they asked, which would a quoll (that had never before experienced a cane toad) prefer to investigate if given the choice: a dead cane toad or a dead mouse? It turned out that the quoll offspring with two toad-exposed parents were somewhat more interested in mice than in cane toads.  The same was true for the hybrids.  However, the toads with two toad-naïve parents showed little preference.

Second, and more important, the researchers gave quolls from the three lines the opportunity to eat a toad leg (which does not have enough poison to harm the quoll). The results of this experiment were striking; offspring of toad-naïve parents were twice as likely to eat the toad leg than were offspring of toad-exposed parents, or hybrids with one parent of each type.


Proportion of toad-naive (both parents toad-naive), hybrid and toad-exposed (both parents toad-exposed) quoll offspring that ate a cane toad leg. Error bar = +/- 1 SE.

Kelly and Phillips conclude that toad-smart behavior is a genetically-based trait that has been under strong natural selection in populations of quolls that survived the cane toad invasion.  Hybrid offspring behave similarly to the offspring of two toad-exposed parents, suggesting that toad-smart behavior has a dominance inheritance pattern. The researchers propose using targeted gene flow, in this case introducing toad-adapted individuals into populations prior to the arrival of cane toads. Recently, Kelly and Phillips released 54 offspring with toad-smart genetic backgrounds onto Indian Island, which is about 40 km from Darwin.  The island has a large cane toad population, so the researchers will follow the introduced quoll population to see whether it is genetically equipped to survive in the presence of the cane toad scourge.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Kelly, E. and Phillips, B. L. (2019), Targeted gene flow and rapid adaptation in an endangered marsupial. Conservation Biology, 33: 112-121. doi:10.1111/cobi.13149. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2019 by the Society for Conservation Biology. All rights reserved.