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Ben Phillips

Tropical Ecology Research Facility

Middle Point, NT

Ph: (08) 8984 9137
Fax: (08) 8984 9139

e-mail: bphi4487@mail.usyd.edu.au

 

  bensoffice

Current Research

Publications


 

Current Research


I am interested in evolution. I just can't seem to get over how amazingly simple yet pleasingly complicated it is. I also have a fondness for reptiles and, I must admit, snakes in particular. These two personality glitches can probably explain my (occasional) presence in the Shine lab.


1. Evolution and Environmental Change

Human-induced environmental change is the greatest threat to global biodiversity.  Such processes include global climate change, invasive species, habitat removal, over-harvesting, and altered biogeochemical cycles.  These changes have caused many extinctions (local and global) and will lead to many more, but whenever the impact is non-random (i.e. selective), there is the potential for adaptive evolution.  Under the right circumstances, adaptive evolution can happen very rapidly in wild populations.  Such “contemporary evolution” occurs as a consequence of selection during natural events.  Importantly however, it has also been documented from “unnatural” (human-mediated) events.  The classic example of industrial melanism in peppered moths is the most celebrated case, however there is also clear evidence of adaptive evolution in populations as a consequence of overfishing, global warming and heavy-metal pollution.

 

These studies highlight the importance of examining the potential for adaptive change in impacted populations.  Doing so can clarify both the nature of the impact and the response of the affected population. Clearly, a population exhibiting an adaptive response is more likely to persist in the face of an environmental change than one that fails to adapt.  Invasive species are of particular interest in this respect, because they constitute a major threat to global biodiversity.  Although invasive species have caused extinctions, they may also exert non-random selection upon impacted species such that the native organisms can adapt to the presence of the invader.



Many species of Australian snake have been severely impacted by the invasion of highly toxic cane toads (Bufo marinus), a conservation problem that also offers an ideal situation to explore the possibility of an adaptive response by natives to an invader.  Cane toads were introduced into Australia in 1935.  Since then they have spread throughout large areas of Queensland and have entered the Northern Territory and New South Wales, currently occupying a range of approximately 1 million square kilometres.  The ecological impact of toads on the native fauna has been poorly elucidated, mainly due to logistical difficulties and a lack of baseline data for comparison.  Nevertheless, there is a clear inference that the invasion of the toad has had a massive impact on species of Australian snakes.  Toads are highly toxic and most Australian snakes attempting to eat toads will die.  In fact, at least 50 species of Australian snake are potentially impacted by toads and the majority of these species are poorly equipped to deal with a likely dose of toad toxin. 


tiolet frog

For the last few years I have been examining the potential for Australian snakes to exhibit an adaptive response to the presence of cane toads.  Results clearly indicate that snakes show increased resistance to toad toxin, decreased preference for toads as prey and adaptive morphological change as a consequence of exposure to toads. These changes appear to be evolved rather than acquired and have happened in less than 70 years (approximately 23 snake  generations).  This suggests that at least some populations of some species will evolve to coexist with toads.  Other populations/species may not.




These results are enough to make one want to run off and become a hippy, but also highlight the importance of acknowledging the potential for adaptive change in conservation planning and management.


 

2. Invasion Biology and the Ecology and Evolution of Cane Toads

In northern Australia, the cane toad front pushes forward at around 55 km per year; more than five times faster than it used to advance when toads were first introduced.  This staggering rate of population advance means that individual toads in northern Australia often move more than 55 km in a year.  There is no other amphibian in the world that comes close to these rates of movement.  Why do toads do this?  Apart from increased mortality associated with increased activity, toads on the invasion front in northern Australia also suffer a heightened prevalence of spinal arthritis as a consequence of their excessive nightly wanderings.  Additionally, it makes very little sense for an amphibian (prone to dessication) to wander off into unknown territory with no guarantee of finding the next waterhole.  So why do they do it? 

My theory is simple: they can't help themselves.  Via a process I term "spatial selection" cane toads on the leading edge of the invasion front have been continually selected for increased dispersal ability.  Why is this so?   If we imagine a population where all the individuals disperse, then reproduce, and then die, and that this population is placed into a large area of suitable vacant habitat, the population will advance its range as individuals disperse.  Importantly, the process of dispersal effectively sorts individuals through space by dispersal ability.  That is, individuals on the edge of the expanding population front are at that edge simply because they dispersed further than other individuals in the population: the process of dispersal has spatially assorted the best dispersers in the population and placed them on the expanding front.  Now, because all the best dispersers are in the same place at the same time, they will tend to breed with each other (the Olympic Village effect).  Thus, if any component of dispersal ability is heritable in this hypothetical species, the offspring of the individuals on the front will tend to have higher dispersal ability than the offspring of individuals from the core of the population.  If we imagine this process occurring every generation as the population expands, the process of spatial assortment for dispersal ability behaves like a runaway evolutionary process, continually selecting for increased dispersal on the advancing front.  Interacting with this process of spatial assortment are density effects.  That is, individuals near the advancing front may benefit from a low density environment (i.e. fewer conspecifics in their vicinity) and, as a consequence, leave more offspring.  Thus, both density effects and spatial assortment on dispersal ability will interact to drive "spatial selection" and the evolution of increased dispersal ability on the expanding edge of range-shifting populations: a truly runaway evolutionary process.

  Universal toad

If all this theory is true (and so far, cane toads are supporting it very nicely), then it may well be true for any species that is expanding its range.  Dispersal ability may always be under strong upward selection when a population expands into suitable habitat.  This has implications for how we assess the impact of climate change.  The simplest way for a species to adjust to climate change is to shift its range so that the species' ditribution is changed but the climatic environment the species experiences is unchanged.  Climate change may wipe out species that cannot shift their range to track climate change, so we need to understand how many species can track climate change and how many cannot.  If dispersal is always selected upwards on the leading edge of an expanding population, then the dispersal rates we measure today may be a poor indicator of the potential rates of dispersal a population can achieve after a few generations of range-shift.

For more information on the latest research on cane toads, visit Rick's website, canetoadsinoz.com

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Publications

Some papers are available as pdf files. To read these you will need Adobe Acrobat Reader.
If you have any difficulties downloading files please contact Mel.

1. Shine, R., B. Phillips, H. Waye, M. LeMaster, and R. T. Mason. 2001. Advantage of female mimicry to snakes. Nature 414:267.
2. Phillips, B. L. 2002. Book Review: The Cane Toad. The history and ecology of a successful colonist. Austral Ecology 27:586.
3. Shine, R., B. Phillips, H. Waye, M. Lemaster, and R. T. Mason. 2003. The lexicon of love: what cues cause size-assortative courtship by male garter snakes? Behavioral Ecology and Sociobiology 53:234-237.
4. Shine, R., B. Phillips, H. Waye, and R. T. Mason. 2003. Small-scale geographic variation in antipredator tactics of garter snakes. Herpetologica 59:333-339.
5. Shine, R., B. Phillips, H. Waye, and R. T. Mason. 2003. Behavioral shifts associated with reproduction in garter snakes. Behavioral Ecology 14:251-256.
6. Phillips, B., G. P. Brown, and R. Shine. 2003. Assessing the potential impact of cane toads (Bufo marinus) on Australian snakes. Conservation Biology 17:1738-1747.
7. Shine, R., B. Phillips, H. Waye, M. Lemaster, and R. T. Mason. 2003. Chemosensory cues allow courting male garter snakes to assess body length and body condition of potential mates. Behavioral Ecology and Sociobiology 54:162-166.
8. Shine, R., B. Phillips, T. Langkilde, D. Lutterschmidt, H. Waye, and R. T. Mason. 2004. Mechanisms and consequences of sexual conflict in garter snakes (Thamnophis sirtalis, Colubridae). Behavioral Ecology 15:654-660.
9.
Phillips, B. L. and M. Fitzgerald. 2004. Encounters between Eastern Brown Snakes (Pseudonaja textilis) and Cane Toads (Bufo marinus) in northern New South Wales. Herpetofauna 34:23-25.
10.
Phillips, B. L., S. J. E. Baird, and C. Moritz. 2004. When vicars meet: a narrow contact zone between phylogeographic lineages of the rainforest skink, Carlia rubrigularisEvolution 58:1536-1548.
11. Dolman, G., and B. Phillips. 2004. Single copy nuclear DNA markers characterised for comparative phylogeography in Australian Wet Tropics rainforest skinks. Molecular Ecology Notes 4:185-187.
12. Phillips, B. L., G. P. Brown, and R. Shine. 2004. Assessing the potential for an evolutionary response to rapid environmental change: invasive toads and an Australian snake. Evolutionary Ecology Research 6:799-811.
13. Shine, R., B. Phillips, H. Waye, M. LeMaster, and R. T. Mason. 2004. Species isolating mechanisms in a mating system with male mate choice (garter snakes, Thamnophis).  Canadian Journal of Zoology 82:1091-1099.
14.
Phillips, B., and R. Shine.  2005.  Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes.  Proceedings of the National Academy of Sciences (USA) 101:17150-17155.
15.
Phillips, B., and R. Shine.  2005.  The morphology, and hence impact, of an invasive species (the cane toad, Bufo marinus) changes with time since colonization.  Animal Conservation 8:407-413.
16.
Smith, J. G., and B. L. Phillips.  2005.  Toxic tucker: assessing the potential impact of cane toads on Australia's reptiles.  Pacific Conservation Biology 12:40-49.
17.
Phillips, B. L., and R. Shine.  2005.  Allometry and selection in a novel predator-prey system: Australian snakes and the invading cane toad.  Oikos 112:122-130.
18.
Phillips, B., and R. Shine.  2005.  Spatial and temporal variation in the morphology (and thus, predicted impact) of an invasive species in Australia.  Ecography 29:205-212.
19.
Greenlees, M. J., G. P. Brown, J. K. Webb, B. L. Phillips, and R. Shine.  2006.  Effects of an invasive anuran (the cane toad, Bufo marinus) on the invertebrate fauna of a tropical Australian floodplain. Animal Conservation 9:431-438.
20.
Phillips, B. L., and R. Shine.  2006.  An invasive species induces rapid adaptive change in a native predator: cane toads and black snakes in Australia.  Proceedings of the Royal Society (London) Series B 273:1545-1550. 
21.
Phillips, B. L., G. P. Brown, J. K. Webb, and R. Shine.  2006.  Runaway toads: an invasive species evolves speed and thus spreads more rapidly through Australia. Nature 439:803.  
22.
Brown, G. P., B. L. Phillips, J. K. Webb, and R. Shine.  2006.  Toad on the road: use of roads as dispersal corridors by cane toads (Bufo marinus) at an invasion front in tropical Australia. Biological Conservation 133:88-94.
23.
Phillips, B. L., G. P. Brown, M. Greenlees, J. K. Webb, and R. Shine.  2007.  Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia. Austral Ecology 32:169-176.
24. Urban, M., B. L. Phillips, D. K. Skelly, and R. Shine.  2007.  The cane toad's (Chaunus marinus) increasing ability to invade Australia is revealed by a dynamically updated range model. Proceedings of the Royal Society (Biological Sciences), London 274:1413-1419.
25. Brown, G. P., C. M. Shilton, B. L. Phillips, and R. Shine.  2007.  Invasion, stress, and spinal arthritis in cane toads.  Proceedings of the National Academy (USA) 104:17698-17700.
26. Greenlees, M. J., G. P. Brown, J. K. Webb, B. L. Phillips, and R. Shine.  2007.  Do invasive cane toads (Chaunus marinus) compete with Australian frogs (Cyclorana australis)?  Austral Ecology 32:900-907.
27. Phillips, B. L., and R. Shine.  2007. When dinner is dangerous: toxic frogs elicit species-specific responses from a generalist snake predator.  American Naturalist 170:936-942.
28. Urban, M., B. L. Phillips, D. K. Skelly, and R. Shine.  2008.  A toad more traveled: the heterogeneous invasion dynamics of cane toads in Australia.  American Naturalist 171:E134-E148.
29. Child, T., B. L. Phillips, G. P. Brown , and R. Shine.  2008.  The spatial ecology of cane toads (Bufo marinus) in tropical Australia: why do metamorph toads stay near the water?  Austral Ecology 33:630-640.
30. Child, T., B. L. Phillips, and R. Shine.  2008. Abiotic and biotic influences on the dispersal behaviour of metamorph cane toads (Bufo marinus) in tropical Australia.  Journal of Experimental Zoology 309A:215-224.
31. Phillips, B. L., J. D. Chipperfield, and M. R. Kearney. 2008. The toad ahead: challenges of modelling the range and spread of an invasive species. Wildlife Research 35:222-234.
32. Kearney, M. R., B. L. Phillips, C. R. Tracy, K. A. Christian, G. Betts, and W. P. Porter. 2008. Modelling species distributions without using species distributions: the cane toad in Australia under current and future climates. Ecography 31:423-434.
33. Phillips, B. L., G. P. Brown, J. M. J. Travis, and R. Shine.  2008.  Reid's paradox revisited: the evolution of dispersal kernels during range expansion.  American Naturalist 172:S34-S48.
34. Barton, K. A., B. L. Phillips, J. M. Morales, and J. M. J. Travis. 2008. The evolution of an 'intelligent' dispersal strategy: biased, correlated random walks on patchy landscapes. Oikos: in press subject to revision.
35. Webb, J. K., G. P. Brown, T. Child, M. J. Greenlees, B. L. Phillips, and R. Shine.  2008.  A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid toxic cane toads.  Austral Ecology: in press.
36. Llewelyn, J., B. L. Phillips, and R. Shine.  2008.  Sublethal costs associated with the consumption of toxic prey by snakes.  Austral Ecology: in press.
37. Alford, R. A., G. P. Brown, L. Schwarzkopf, B. Phillips, and R. Shine.  2008.  Comparisons through space and time suggest rapid evolution of dispersal behaviour in an invasive species.  Wildlife Research: in press.
38. Hagman, M., B. L. Phillips, and R. Shine.  2008.  Tails of enticement: caudal luring by an ambush-foraging snake (Acanthophis praelongus, Elapidae).  Functional Ecology: in press.
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