Introduced quolls quell melomys

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

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

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

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

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

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

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

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

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

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

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

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

Figure 4

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

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

Figure 5B

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

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

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

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

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