Introduced quolls quell melomys

October 25, 2021 by fredsingerecology

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

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

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

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

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

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

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

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

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

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

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

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

Figure 4

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

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

Figure 5B

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

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

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

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

Australian eruptions

March 25, 2021 by fredsingerecology

Red foxes were introduced to Australia in the mid-19^th 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.

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.

Fewer infections found in forest fragments

June 27, 2019 by fredsingerecology

As human populations expand, we are converting ecosystems from one state to another. In the case of tropical forests, conversion of forest to cropland may leave behind fragments of relatively undisturbed forest surrounded by a matrix of cropland or other forms of development. Conservation ecologists are exploring whether ecological processes and ecosystem structure in these fragments work pretty much like normal forested regions, or whether fragments behave differently. To do this, in a few locations around the world such as the Wog Wog Fragmentation Experiment in New South Wales, Australia, researchers have systematically created forest fragments of various sizes. They can then ask a variety of questions comparing fragments vs. intact forest. For example, how does species diversity, or how do processes such as competition, predation and mutualism differ in the two landscapes?

Aerial photo of Wog Wog Fragmentation Experiment at the time the experiment began in 1987. Credit: Chris Margules.

Julian Resasco was working as a postdoctoral associate in Kendi Davies’ lab at the University of Colorado on a study that looked at changes in invertebrate communities in response to fragmentation at Wog Wog. Beginning in 1985, researchers had set up a network of pitfall traps, which are cups that are buried with their tops level to the ground, so that any careless organism that wanders in will be trapped in the cup. Some pale-flecked garden skinks, Lampropholis guichenoti, also had the misfortune to become entrapped and became subjects for the study. The invertebrates, and the 186 unfortunate skinks were preserved in alcohol and stored as part of the Australian National Wildlife Collection.

Skink museum specimens at the Australian National Wildlife Collection. Credit: Julian Resasco.

Much later, Resasco arrived and began dissecting skink guts to analyze the prey items for a study that looked at how the skinks shifted prey consumption (their feeding niche) in response to fragmentation. While dissecting the skink guts, he noticed that some of the skinks had worms (nematodes) inside their guts. These nematodes were relatively common among skinks from continuous eucalypt forests, rare among skinks from eucalypt fragments, and absent from skinks in the cleared, pine plantation matrix.

Top. The study area in southeast Australia, showing location of continuous forest, forest fragments and surrounding matrix. Dots indicate locations of pitfall traps. The matrix was planted in pine seedlings soon after fragmentation. Bottom. The pale-flecked garden sunskink Lampropholis guichenotti. Credit: Jules Farquar

As it turned out, the nematode was a new species, which Resasco and a colleague (Hugh Jones) named Hedruris wogwogensis. Nematodes in the genus Hedruris use crustaceans as intermediate hosts, which alerted Resasco and his colleagues that the terrestrial amphipod Arcitalitrus sylvaticus, which was very common in the pitfall traps, was probably an important intermediate host. When amphipods from pitfall traps were examined microscopically, a small portion of them were infected with Hedruris wogwogensis. The researchers concluded that amphipods became infected when they ate plants that harbored nematode eggs or young nematodes, which then developed in amphipod guts, and were passed on to skinks that ate the amphipods. Thus somewhat inadvertently, one aspect of the study transitioned into the question of how fragmentation can influence the transmission of parasites.

After concluding their skink dissections, Resasco and his colleagues discovered that skinks in continuous forest had five times the infection rate as did skinks in fragmented forest. In addition, no skinks collected in the matrix were infected. Infected skinks harbored a similar number of nematodes, whether they lived in continuous forest or fragments (see the Table below). Lastly, amphipods were considerably more common in skink guts and pitfall traps from continuous forest, less so in fragments, and least in the matrix.

Summary of data collected by Resasco and his colleagues. Nematode intensity is the mean number of nematodes per infected skink. Nematode abundance is the mean number of nematodes per skink (infected and uninfected).

The researchers put these findings together in a structural equation model. The boxes in the model below represent the variables, while the numbers in smaller boxes over the arrows are the regression coefficients, with larger positive numbers (in black) indicating stronger positive effects, and larger negative numbers (in red) indicating stronger negative effects. The model revealed three important findings. First, habitat fragmentation strongly reduced amphipod abundance. High amphipod abundance was associated with high nematode abundance (that is the +0.20 in the model), so lower amphipod abundance from fragmentation reduced nematode abundance. Second, habitat fragmentation positively affected skink abundance – more skinks were captured in fragments than in intact forest, but this increase had no effect on nematode abundance in skinks. Finally, note the direct arrows connecting “Fragmentation” to “Log nematode abundance in skinks”. This indicates that other variables (beside amphipod abundance) are reducing infection rates in skinks that live in fragments and the matrix.

Structural equation model showing effects of fragmentation on nematode infection in skinks. Amphipods are the intermediate host. Black arrows indicate significant positive effects of one variable on the other, while red arrows indicate significant negative effects. Solid lines represent fragments compared to controls and dashed lines represent the matrix compared to controls. Thicker lines are stronger effects.

At this point, we still have an incomplete understanding of the system. We know that fragmentation reduces amphipods, which require a moist and shaded environment to thrive. Reduced amphipod abundance leads to lower nematode infection rates in skinks. But we know that other variables are important as well; perhaps nematodes survive more poorly in fragment and matrix soils. Interestingly, pine trees were planted in the matrix and are beginning to mature and shade out the matrix environment. Amphipod abundances are on the rise, so the researchers predict that nematode infection rates will begin to increase accordingly. Those studies have begun.

Eucalypt forest canopy at Wog Wog. Credit: Julian Resasco.

Looking at the bigger picture, it is clear that fragmentation may decrease (as in this study) or increase the abundance of an intermediate host. As an example of fragmentation increasing intermediate host abundance, the researchers describe a study in which fragmentation increased the abundance of the white footed mouse, an intermediate host for black-legged ticks (that host the bacteria that causes Lyme disease). We need to unravel the connections between landscape factors and the various species they influence, so we can begin to understand how human changes to the landscape can influence the transmission of diseases.

note: the paper that describes this research is from the journal Ecology. The reference is Resasco, J., Bitters, M. E., Cunningham, S. A., Jones, H. I., McKenzie, V. J., and Davies, K. F.. 2019. Experimental habitat fragmentation disrupts nematode infections in Australian skinks. Ecology 100( 1):e02547. 10.1002/ecy.2547. 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.

Quoll vs. toad: a toxic brew

May 6, 2019 by fredsingerecology

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.

Predators and livestock – “stayin’ alive.”

January 24, 2018 by fredsingerecology

President Donald Trump was elected on a platform that included building a great wall whose purpose was to keep out unwanted intruders from the south, and that would be paid for (apparently magically) by these same intruders. The idea of building a great wall has been around for a long time; the Great Wall of China was constructed over a time period of almost two thousand years to keep out unwanted intruders (this time from the north). Not surprisingly, the cost of that Great Wall was not borne by the unwanted intruders. More recently, in the 1880s, the government of Australia constructed a 5500 km fence designed to keep unwanted dingoes away from sheep that pasture in southeastern Australia. As Lily van Eeden describes, the Australian government spends about $10 million dollars per year to maintain the fence but there are almost no data to compare livestock losses on either side of the fence. Thus she and her colleagues decided to look at what was being done globally to evaluate the effectiveness of different methods of protecting livestock.

The Dingo fence across southeastern Australia. Credit Peter Woodard.

The researchers grouped livestock protection approaches into five different categories: lethal control, livestock guardian animals such as dogs, llamas and alpacas, fencing, shepherding and deterrents. Lethal control includes using poison baits and systematic culling of populations of top predators. Deterrents include aversive conditioning of problem predators, chemical, auditory or visual repellents, and protection devices such as livestock protection collars.

A guardian dog emerges from the midst of its flock in Bulgaria. Credit: Sider Sedefchev.

Van Eeden and her colleagues then did a meta-analysis to see which approach worked best. You can check out my blog from Aug. 2, 2017 (“Meta-analysis measures multiple mycorrhizal benefits to plants”) for a more detailed discussion of meta-analyses. Very briefly a meta-analysis is a systematic analysis of data collected by many other researchers. This is challenging because each study uses slightly different techniques and has different levels of rigor. For this meta-analysis, van Eeden and her colleagues used only two types of studies. One type is a before/after design, in which researchers kept data on livestock loss before the mitigation treatment as well as after. The second type is a control-impact design, in which there was a control group set aside, which did not receive the mitigation treatment. Each study also needed sample sizes (number of herds and/or number of years), means and standard deviations, and had to be run for at least two months to be used in the meta-analysis.

The researchers searched several databases (Web of Science, SCOPUS and European Commission LIFE project), Google Scholar, and also used more informal sources, to collect a total of more than 3300 records. However, after imposing the requirements for types of experimental design and data output, only 40 studies remained for the meta-analysis. Based on these data, all five mitigation approaches reduced predation on livestock. The effect size in the figure below compares livestock loss with the treatment to livestock loss without the treatment, so that a negative value indicates that the treatment is associated with reduced livestock loss. The researchers conclude that all five approaches are somewhat effective, but the large confidence intervals (the whiskers in the graph) make it difficult to unequivocally recommend one approach over another. The effectiveness of lethal control was particularly variable (hence the huge confidence interval), as three studies showed an increase in livestock loss associated with lethal control.

Mean effect size (Hedges’ d) and confidence intervals for five methods used to mitigate conflict between predators and livestock. More negative effect size indicates a more effective treatment. Numbers in parentheses are number of studies used for calculating mean effect size.

Finding that non-lethal management is as effective (or possibly more effective) than lethal control tells us that we should probably be very careful about intentionally killing large carnivores, since, in addition to being cool animals that deserve a right to exist, they also perform some important ecosystem services. For example, in Australia, there are probably more dingoes northwest of the fence than there are south of the fence, so exclusion may be working. However there is some evidence that there are also more kangaroos and rabbits south of the fence, which could be an unintended consequence of fewer predatory dingoes. Kangaroos and rabbits eat lots of grass, so keeping dingoes away could ultimately be harming the sheep populations. Dingoes may also kill or compete with invasive foxes and feral cats, which have both been shown to drive native species to extinction, so excluding dingoes may increase foxes and cats, threatening native species. Van Eeden and her colleagues argue that different mitigation approaches work in different contexts, but that we desperately need evidence in the form of standardized evaluative studies to understand which approach is most suitable in a particular context.

Context-specific approach to managing the co-exstence of predators and livestock.

In all contexts, cultural and economic factors interact in mitigating conflict between humans and carnivores. The dingo is officially labeled as a wild dog, which invaded Australia relatively recently (about 4000 years ago), so the public perception is that this species has a limited historical role. Other cultures may have a different view of their predators. For example, the Lion Guardian project in Kenya, which trains and supports community members to protect lions, has successfully built tolerance for lions by incorporating Maasai community cultural values and belief systems.

To use a phrase that President Trump recently forbade the Centers for Disease Control to use in their reports, our decisions about predator mitigation should be “evidence-based.” We need more controlled studies that address the success of different mitigation approaches in particular contexts. We also must understand the costs of removing predators from an ecosystem, as predator removal can initiate a cascade of unintended consequences.

note: the paper that describes this research is from the journal Conservation Biology. The reference is van Eeden, L. M., Crowther, M. S., Dickman, C. R., Macdonald, D. W., Ripple, W. J., Ritchie, E. G. and Newsome, T. M. (2018), Managing conflict between large carnivores and livestock. Conservation Biology, 32: 26–34. doi:10.1111/cobi.12959. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2018 by the Society for Conservation Biology. All rights reserved.

Cat and fox: agents of Australian extinctions

November 15, 2017 by fredsingerecology

Seagrass scourge: when nutrient enrichment reaches the tipping point

October 24, 2017 by fredsingerecology

Sean Connell has watched as south Australia has lost vast expanses of kelp forest and seagrasses over the past years. One of the primary culprits associated with loss of seagrass meadows is excessive nutrients, particularly nitrogen, which enters the ecosystem with runoff, and causes an increase in algal epiphytes (epiphytes are small plants that grow on other plants). Epiphytes can negatively affect seagrass by blocking sunlight needed for photosynthesis, and indirectly, by increasing the rate of cellular respiration within the ecosystem, thus using up oxygen needed by seagrass for metabolic processes.

Two dolphins swim above a bed of seagrass off the south Australian coast.

Connell and his colleagues noticed that seagrass loss was often sudden; a large seagrass meadow would appear to be in good shape, and then it would abruptly disappear. They suggested that there might be a threshold effect in nutrient levels that seagrasses can tolerate; that these systems function well until a certain threshold in nutrient levels is crossed, above which there is an abrupt loss of seagrasses. They tested this hypothesis by subjecting plots of the seagrass Amphibolis antarctica to seven different concentrations of dissolved inorganic nitrogen (DIN) over a 10 month period, and monitored the abundance of epiphytes and seagrass over that timespan.

The meadows were about two km offshore from Lady Bay, Fleurieu Penninsula, Australia, in about 5 meters of water. Different amounts of nitrogen fertilizer were wrapped in nylon bags (for slow continuous release of DIN) and staked to the ocean floor. Amphibolis antarctica grows by producing new leaves at the top of each leaf cluster, but at the same time it drops old leaves. Leaf turnover, the researchers’ measure of growth, is simply new leaf production minus old leaf drop. The researchers tied on a small nylon cable at known locations on selected plants, noted how many leaves were above and below each tie at the beginning of the experiment, and recounted leaf number 10 months later. Finally, the researchers measured epiphyte growth by microscopically viewing a sample of seagrass leaves, and counting the number seagrass leaf cells that were covered by epiphytes.

Seagrass growth was relatively unaffected by all tested DIN levels.

Leaf production per day in relation to concentration of DIN.

However, leaf drop showed a strong threshold effect; leaf drop rates increased sharply between 0.13 – 0.15 mg/L of DIN.

Leaf drop per day in relation to concentration of DIN.

Putting these two graphs together, you can see (below) that leaf turnover switched from positive to negative at 0.13 – 0.15 mg/L of DIN. Negative leaf turnover translates to a sudden loss of seagrass at that threshold. At least in this system, at this location, 0.13 – 0.15 mg/L of DIN is the tipping point, beyond which the seagrass system suddenly goes into decline.

Leaf turnover per day (left y-axis and red data), and Epiphyte cover (% – right y-axis and green data), in relation to concentration of dissolved inorganic nitrogen.

The graph also shows that the tipping point coincides with an epiphyte cover of approximately 60%. It is possible that increased epiphyte cover may reduce seagrass photosynthetic rates (particularly in lower leaves), so that leaf turnover suddenly shifts into the negative zone, but the study was not designed to identify the underlying mechanism.

Seagrass meadows perform important ecosystem services, such as absorbing excess nutrients from the sediment, and providing habitat and food for a diverse group of grazers and indirectly, for their consumers. Thus seagrass conservation is vital. The danger here is that moderate levels of nutrients do not appear to have much effect on seagrass populations, but there is an abrupt shift to seagrass loss once the nutrient threshold is crossed. This makes the system very difficult to manage, because the loss occurs without warning. Australian ecologists have repeatedly failed to restore lost seagrass meadows, as simply reducing nutrient levels does not reverse the process. Thus anticipating seagrass loss before it happens is the most viable management solution for this critical ecosystem.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Connell, S. D., Fernandes, M., Burnell, O. W., Doubleday, Z. A., Griffin, K. J., Irving, A. D., Leung, J. Y.S., Owen, S., Russell, B. D. and Falkenberg, L. J. (2017), Testing for thresholds of ecosystem collapse in seagrass meadows. Conservation Biology, 31: 1196–1201. doi:10.1111/cobi.12951. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2017 by the Society for Conservation Biology. All rights reserved.

Frogs face fatal fungal foes

June 25, 2017 by fredsingerecology

Pathogens are organisms that cause disease, and like all organisms, they obey evolutionary principles. Pathogens that survive and reproduce successfully in a particular environment will have more offspring than those that are less successful, thereby passing on those traits that promote successful reproduction to future generations. The problem is that many pathogens change their environment in a way that makes their environment less hospitable for their own survival or reproduction. For example, the fungal pathogen Batrachochytrium dendrobatidis (Bd) causes chytridiomycosis in its amphibian host, which may severely reduce the host population size to the point where few individuals survive. If the host population goes extinct, then there are no hosts for the fungal offspring to infect.

Scanning electron micrograph of Batrachochytrium denbdrobatidis spore. Credit: Dr. Alex Hyatt, CSIRO Livestock Industries’ Australian Animal Health Laboratory.

Fortunately for Bd, but unfortunately for amphibians, there are several ways out of this conundrum. One approach is a reduction in pathogenicity so that a pathogen’s host species is able to tolerate the infection (and of course, natural selection will at the same time favor an increase in the host species’ tolerance for the pathogen). A second approach is to broadcast a wide net by infecting many different species. That way if one host species goes extinct, there are always many other species to infect. Bd infects over 500 species of amphibians, and has been implicated in the extinction of over 100 amphibian species, and the severe decline of an additional 100 species.

Ben Scheele and his colleagues wanted to know why the endangered northern corroboree frog, Pseudophryne pengilleyi, was declining in southeastern Australia. Several previous studies showed that many corroboree frog populations declined or went extinct in that region over the past 20 years, while the abundant common eastern froglet, Crinia signifera, showed no signs of decline over the same time period. Pilot studies showed that eastern froglets were heavily and commonly infected with Bd. The researchers reasoned that eastern froglets could be acting as a reservoir for Bd, so that corroboree frog populations are being decimated by association with Bd-infected eastern froglets.

Female Pseudophryne pengilleyi. Credit: David Hunter.

Preliminary surveys indicated that the decline of corroboree frogs was not uniform across the study site; in fact there were some newly discovered populations that were doing very well. The researchers defined three types of sites in their research area. Absent sites (40 in total) had corroboree frogs in 1998, but the population went extinct by 2012. Declined sites (17 in total) had a greater than 80% decrease in abundance since 2000. New sites (25 in total) were newly discovered since 2012, and had much higher population densities than declined sites.

Study area in southeastern Australia, showing locations of Absent, Declined and New sites.

Unfortunately, it is impossible to visually distinguish an infected frog from an uninfected frog, at least until the few hours before death. But the researchers needed to be able to tell if a frog had chytridiomycosis. So they collected skin swabs from the frogs during the breeding season – only working at night to ensure cool humid conditions which minimized frog stress. They then did real time PCR on these samples to quantify the intensity of Bd infection.

Scheele and his colleagues had three important questions they were now prepared to answer. First, how prevalent is Bd in these two species? They found that infection rate was much higher in eastern froglets (79.4%) than in corroboree frogs (27.3%). The intensity of infection (measured by the number of fungal spores) was also much greater in eastern froglets than in corroboree frogs.

Second, do eastern froglets act as a reservoir for Bd, leading to infection and decline of corroboree frog populations? As we discussed earlier, the two species coexist at some sites, but not at others. If eastern froglets act as a reservoir for Bd, we would expect corroboree frogs to have higher infection rates at sites they share with eastern froglets, than they do at sites without eastern froglets. In support of this prediction, Bd prevalence in corroboree frogs was 41.4% at sites with eastern froglets, but only 2.6% at sites with no eastern froglets.

C. signifera (left) and P. pengilleyi spending quality time together in a P. pengilleyi nest. Credit: David Hunter.

Finally, the researchers want to identify conditions that will promote corroboree frog recovery. They approached this quantitatively by modeling the probability of a site being classified as Absent, Declined or New, in relation to eastern froglet abundance. Based on their survey data of 81 sites, those sites with the highest eastern froglet abundance are most likely to be classified as Absent (corroboree frog extinction), while sites with very few eastern froglets are most likely to be classified as New (thriving corroboree frog populations).

Probability of a site being classified as Absent, Declined or New, based on eastern froglet abundance. Data are log transformed. Dashed lines are 95% confidence intervals.

Scheele and his colleagues conclude that eastern froglets are a reservoir host for Bd, and have played a major role in the decline in corroboree frog populations. The researchers point out that, in general, areas lacking reservoir hosts may provide endangered species with refugia from infectious disease. For managing endangered species, conservation biologists should carefully monitor sites for the presence of reservoir hosts so they don’t reintroduce rare and endangered animals into locations where they will be attacked and killed by pathogens.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Scheele, Ben C., David A. Hunter, Laura A. Brannelly, Lee F. Skerratt, and Don A. Driscoll. “Reservoir‐host amplification of disease impact in an endangered amphibian.” Conservation Biology 31, no. 3 (2017): 592-600. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2017 by the Society for Conservation Biology. All rights reserved.

Metallic starlings: a rain of terror

February 22, 2017 by fredsingerecology

I am a slow learner. Several times in the past few years I have paddled my canoe under a particular sycamore tree in the New River in Radford, Virginia. Each time I do so, I am greeted by large numbers of cormorant poop bombs dropped by the dozens of cormorants that seem to find that particular tree to their liking, and this particular canoeist not to their liking. Fortunately, cormorants have bad aim, but unfortunately it is not that bad.

Daniel Natusch and three other researchers wanted to know how an analogous form of nutrient enrichment from large colonies of nesting Metallic Starlings (Aplonis metallica) affects the nearby ecosystem in a tropical Australian rainforest. They were interested in this question because it was obvious that the ground below the nesting colony trees was basically devoid of vegetation; they describe it as “an open moonscape”, contrasting sharply with the thick rainforest nearby. Other studies have shown that nutrient enrichment from bird guano leads to increased vegetation density – so why is this ecosystem different?

Lockerbie Scrub rainforest, in Cape York Peninsula, Australia, showing colony tree with dead zone (left) and a continuous rainforest (right)

Dan Natusch conducts herpetological research with his son Huxley. Credit: Jessica Lyons

The researchers compared the biological, chemical and physical environment underneath 27 different colony trees to the environment underneath a randomly chosen tree 100-200 meters from the colony tree. As expected, they found very little vegetation near colony trees, in contrast to relatively dense vegetation near the randomly chosen trees.

Vegetation cover (left) and number of live stems (right) in relation to distance from the colony or randomly chosen tree (Point 0 on X-axis). Negative numbers are downslope and positive numbers are upslope from the tree.

Soil analyses showed that the soils under the colony trees had much higher concentrations of important nutrients. For example, phosphorus levels were more than 30 times greater, and ammonium nitrogen was about four times greater under colony trees than under the randomly chosen trees. The researchers wondered whether these nutrient levels were so high that they were toxic to vegetation. That would account for the dead zone under the colony trees. An alternative hypothesis is that animals (pigs and turkeys in particular) may be attracted to these high nutrient areas under the colonies, and may either kill germinating plants by eating or trampling them.

: Feral pigs (Sus scrofa) rooting and trampling under a colony tree. Credit Daniel Natusch

To test both hypotheses, at the beginning of the breeding season the researchers covered a portion of the colony tree region with metal cages (exclosures) that prevented turkeys and pigs from gaining access. They discovered a much greater number of seedlings under the exclosures in comparison to the areas where turkeys and pigs could access the seedlings.

natuschfig7 They concluded that nutrient levels were not toxic to seedlings, but that pigs and turkeys were either eating or trampling the seedlings as they emerge. As you can see, the number of exclosure seedlings dropped sharply in July, in part because rainfall declines sharply in June, which leads to high plant mortality, particularly in the unshaded dead zone. But in addition, feral pigs broke into all of the exclosures that summer to access the seedlings and the nutrient-rich soil.

Do these dead zones actually benefit the starlings in any way? One possible advantage is that dead zones prevent snakes from climbing nearby trees and vines to gain access to the nests that are located high in the canopy of the colony tree. However there is good evidence that colony trees suffer high mortality, as 10 of the 27 colony trees died within three years of the study. Trees that fall during the nesting period could lead to the failure of all of the nests within that colony tree.

A scrub python (Morelia amethistina) puts the squeeze on a juvenile Metallic Starling. Credit Daniel Natusch.

Why do we find dead zones beneath colonies of Metallic Starlings, and increased plant growth rate, larger plant size and greater plant diversity beneath the colonies of several other bird colonies? Most previous studies have looked at sea-bird colonies on small islands that have few terrestrial herbivores, so germinating seedlings are relatively undisturbed. This study occurred in a continuous forest in tropical Australia, which harbored a large population of hungry herbivores. These contrasting findings show the important role of environmental context for understanding how ecological interactions will play out. Given that we humans are continually adding nutrients to our environment (through natural bodily function and when we fertilize our fields), we need to carefully consider the biotic and abiotic players in the ecosystem, so we can predict the effects we are having on the environment.

note: the paper that describes this research is from the journal Ecology. The reference is Natusch, D. J. D., Lyons, J. A., Brown, G. P., & Shine, R. (2017). Biotic interactions mediate the influence of bird colonies on vegetation and soil chemistry at aggregation sites. Ecology 98(2): 382-392. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.

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