Discussion Paper |
Corresponding author: Benjamin D. Hoffmann ( ben.hoffmann@csiro.au ) Academic editor: Ingolf Kühn
© 2016 Benjamin D. Hoffmann, Franck Courchamp.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Hoffmann BD, Courchamp F (2016) Biological invasions and natural colonisations: are they that different? NeoBiota 29: 1-14. doi: 10.3897/neobiota.29.6959
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We argue that human-mediated invasions are part of the spectrum of species movements, not a unique phenomenon, because species self-dispersing into novel environments are subject to the same barriers of survival, reproduction, dispersal and further range expansion as those assisted by people. Species changing their distributions by human-mediated and non-human mediated modes should be of identical scientific interest to invasion ecology and ecology. Distinctions between human-mediated invasions and natural colonisations are very valid for management and policy, but we argue that these are value-laden distinctions and not necessarily an appropriate division for science, which instead should focus on distinctions based on processes and mechanisms. We propose an all-encompassing framework of species range expansion. This does not detract from the importance of invasion biology as a discipline, but instead will help bring together research being conducted on multiple taxa, and by multiple disciplines, including epidemiology, that are often focused on an identical phenomenon: colonisation.
Alien, biological invasion, colonisation, dispersal, exotic, invasion, introduction
Ecologists studying human-mediated biological invasions and those studying natural colonisations are essentially working on the same phenomenon (
Following are four examples of the irrelevance of dispersal mode for the science of colonisation. The first is the Lessepsian migration: the dispersal of at least three hundred species from the Red Sea into the Mediterranean Sea following the opening of the Suez Canal. Most species have increased their distributions naturally, as the dominant currents and winds have dispersed their propagules northward (
The second example is the 2011 Tohoku tsunami, which carried about 1.5 million tonnes of debris, vegetation and fauna out to sea. The flotsam was carried across the Pacific where it was also colonised by other marine flora and fauna, and some reached North American coastlines nearly 8,000 kilometres away (
A more tangential and arguably extreme example would be the greatest colonisation in global history: humans. Ecologists now accept that people are not disconnected from the environment, and thus scientific understanding of our own spread across the globe cannot be isolated from that of all other species. However, it can certainly be argued that our own dispersal was human mediated, and caused great impact in new ecosystems, which would qualify as an invasion. Yet, certainly in pre-historic times our survival and further spread was fully compliant with, and restricted to, the rules of nature, which would qualify as a colonisation. So did humans naturally colonise the globe, or were we a biological invasion? We argue that the distinction is extraneous semantics: we were both, because both terms describe the same phenomenon.
The last example is the myriad of species undergoing range-shifts due to climate change, which is an issue that is set to result in even less clarity of what is an “exotic” species (
Despite several papers over multiple decades highlighting the lack of distinction between “invasions” and colonisations from an ecological perspective (
The first argument against ending the artificial separation between colonisation and invasion is that propagule pressure is greater for species dispersed by human mediation, and therefore this represents a difference in process. Propagule pressure consists of the number of individuals arriving in a new location at one time and the number of arrival times. Although we now have good data of accidental human-mediated propagule pressure from the likes of shipping ballast, and cargo freight, the same cannot be said for natural colonisation. As far as we are aware, no attempt has ever been made to compare propagule pressure in any location between natural dispersal events and human-mediated dispersal. But if such a comparison was made, we suspect that on a global-scale, propagule pressure would often be comparable for species dispersing naturally. For example, it has been estimated that 4.5 billion insects were dispersed over the North Sea each summer day from a 30 km coastal strip alone (
The second argument is that colonisation pressure (the number of species introduced per colonisation event) is greater for species spread by human mediation, and therefore this is a difference in process. While we agree that such a discrepancy is likely for fauna that clearly cannot easily disperse biogeographically (e.g., lizards, land snails, frogs), the same may not necessarily be so for the bulk of species, the invertebrates, as detailed above. However, such a comparison may not necessarily be meaningful, because natural colonisations appear to occur over continuous periods, not necessarily just individual events (e.g., a cyclone). Just as for propagule pressure, as far as we are aware, there has never been an attempt to compare colonisation pressure in any one location from human-mediated dispersal versus natural dispersal, but disjunct data do exist for comparison. For example, for natural colonisations, within the first two years of the eruption of Mt. St. Helens, USA, in 1980, 43 spider species had ballooned in, including three European species (
A third argument is that natural and human-mediated dispersal result in differences in genetic diversity that affect colonisation success, largely being that greater propagule pressure from human-mediated dispersal can result in greater genetic diversity. But there are many documented instances where invasions arose from a very small propagule. For example, the thousands of feral cats than now invade the Kerguelen Islands come from only 2 to 4 cats (
We agree that higher propagule pressure increases the likelihood of colonisation success (
Importantly for these three arguments, and possibly others, comparisons between species movement by human mediation and natural dispersal must be equivalent comparisons whereby only a single factor varies, but this is often not the case. For example, it is not valid to argue that there are genetic differences when comparing the deliberate introduction of a grass, whereby thousands of seeds with great genetic diversity are brought to an area, with the natural dispersal of a single seed because in this instance genetics is confounded with different levels of propagule pressure.
The fourth argument is that invasions, unlike colonisations, are drivers of mass-extinction. We have four issues with this argument. First, implicit in this argument is that natural colonisations don’t have negative impacts, and they are not responsible for localised extinctions. We are unaware of a naturally dispersed species being reported as causing an extinction, but perhaps this is due to the difficulty of demonstrating that a species has indeed self-dispersed and not been spread by human means and then caused an extinction of a native species. Logically, however, throughout evolutionary time, as species have arisen and dispersed, and as species distributions have changed following climates and tectonic movements, they have outcompeted and replaced other biota. For example, placental mammals outcompeted marsupials throughout most of the world. This is particularly well studied in the multiple waves of migrations of mammals between North and South America as the Isthmus of Panama rose c. 3–10 Mio. years ago that resulted in the replacement of most of South America’s mammals (Great American Interchange) (
Many frameworks have been proposed that attempt to display the theoretical processes of biological invasions (
Despite the advance provided by Blackburn’s invasion framework, we believe that it stops short of being more widely applicable for ecology because it solely considers species movements that are human-mediated, and therefore colonisation, even at the biogeographic scale, is excluded (
The colonisation framework. This framework considers both human-mediated dispersal and natural dispersal, and acknowledges that any species in novel environments are subject to the same barriers of survival, reproduction, dispersal and further range expansion, irrespective of how they got there. This framework is relevant for epidemiology, simply by changing a few terms (e.g., species movement to infection, dispersal to transmission, invasion to disease spread).
The framework presented here differs from that in
Both with and without the context of climate change, using the framework to detail colonisations overrides subjective issues defining exotics, such as distance away from a species’ historic distribution, recolonisation of extinct populations and colonisation without evolutionary history.
Blackburn’s framework was based on synergies of terrestrial plants and animals. Already the framework has proven applicable for marine animals (
Finally, this framework more easily allows the exchange of research ideas and findings across biological disciplines (e.g., conservation biology, invasion ecology, island ecology and biogeography, epidemiology) and for different focal taxa or biomes (e.g., microorganisms, plants and animals, marine and terrestrial organisms) that are often focused on the same phenomenon – colonisation. In particular, for invasion biology, possibly more so than for other science disciplines, the isolation of researchers focused on different taxa or biomes, and researchers from managers, has resulted in the loss of clear definitions and vast inconsistencies in terminology (Heger et al. 2013;
There is no doubt that dispersal mode greatly influences the opportunity for species to disperse (
We argue that climate change biologists, invasion biologists, restoration ecologists, island biogeography biologists, community assembly ecologists and epidemiologists are unnecessarily conducting research in isolation from each other despite essentially studying the same phenomenon – colonisation. Biological invasions do not represent a distinctly different or change in process, just an acceleration of the colonisation process through multiple mechanisms. The major difference between invasion and colonisation stands, we believe, on ethical ground. This difference should not dictate the science, only management and policy making. For biological invasions, we believe that predictive understanding would benefit most greatly from focusing on (1) determining why so many more species do not manage to successfully colonise new areas (
We thank many people for stimulating discussions about aspects of this paper, especially, Tim Blackburn, Phil Hulme, and Carol Lee. BDH thanks the Ecologie, Systématique et Evolution laboratory at the University of Paris Sud for hospitality. FC was funded by Biodiversa EraNet, BNP Parisbas and ANR grants.