The Nature of the Problem. Those of us alive today are witness ing the consequences a number of truly grand, but unplanned, biological experiments. They are the result of the activities of a massive human population that is still growing and increasing its impact on the Earth. Because there are no controls on these experiments, as such, we must look to biological patterns through time for perspective on the consequences of the mixing of biotas. This is a challenge because environments of the past also changed, sometimes abruptly.
These historical fluctuations in climate and biota of the past have led some to say that nothing new is happening that has not already happened before. The response to this proposition is yes, but the rate of change
in the composition of the atmosphere today exceeds anything of the past, as will the consequent rate of climate change. This is also true to a large degree in the extent of migration of species among continents. Before the Age of Exploration, dispersal of organisms across these great biogeographic barriers was a low-probability event; however, today this is routine. In this paper we briefly summarize the consequences of the massive movement of organisms across these barriers in terms of the course of future evolution.
We start this essay with two quotes providing perspectives on the problem. One is from the pioneering work of Charles Elton (1), who stated, "We must make no mistake: we are seeing one of the great historical convulsions in the world's fauna and flora." Elton certainly had no doubts of the magnitude of the invasive species issue. More recently, Geerat Vermeij (2) remarked specifically about the evolutionary consequences of this convulsion, "... if newcomers arrive from far away as the result of large-scale alterations in geography or climate, the change in selective regime and the evolutionary responses to this change could be dramatic." We examine here some of the evidence for this potentially dramatic scenario.
The Changing Evolutionary Landscape. It is commonly acknowledged that the abiotic environment is being greatly altered because of massive land-use alteration and emerging climate change (3, 4). However, an equally drastic alteration is occurring in the composition of biotic communities. The kinds of physical and biotic environments that exist now are quite different from those that have existed in recent geological times.
International commerce has facilitated the movement of species; this is true globally and across taxonomic groups. Ironically, this has increased species richness in many places where new species are introduced. The actual numbers of individuals and species being transported across biogeographical barriers every day is presumably enormous. However, only a small fraction of those transported species become established, and of these generally only about 1% become pests (5). Over time however, these additions have become substantial. There are now as many alien established plant species in New Zealand as there are native species. Many countries have 20% or more alien species in their floras (6). There are few geographic generalities to these trends; the strongest is that islands, in particular, have been the recipients of the largest proportional numbers of invaders. Biotic homogenization within continents is equally as striking as mixing among oceans. As one example, Rahel (7) notes that in the United States pairs of states on average now share 15 more species than they did before European settlement. The states of Arizona and Montana, which previously had no fish species in common, now share 33 species in their faunas.
Mack (8) estimates that over the last 500 years, invasive species have come to dominate 3% of the Earth's ice-free surface. Vast land or waterscapes, in certain regions, are completely dominated by alien species, such as the star thistle Centaurea solstitialis in the rangelands of California, cheatgrass (Bromus tectorum) in the intermountain regions of the western United States, and water hyacinth (Eichornia crassipes) in many tropical lakes and rivers.
The Rates of Exchange. As the volume of global trade increases, one would expect the rate of establishment of alien species to increase also; data support this prediction. Cohen and Carlton (9) noted that the rate of invasion into San Francisco Bay has increased from approximately one new invader per year in the period of 1851-1960, to more than three new invaders per year in the period of 1961-1995. In the United States the numbers of fish introductions, either from foreign sources or across watershed boundaries, has increased dramatically. In the period between 1850 and 1900, 67 species were introduced, between 1901 and 1950, 140 species, and between 1951 and 1996, 488 species (ref. 10 and the web site referred to therein).
In addition to the greater number of species crossing borders there is also a buildup in the invasive potential of those nonnative species already established in a region, as immigration increases their population sizes. "Introduced species" may stay at a fairly low population size for years and then explode at some later date
the so-called lag effect. This lag effect may simply be the result of the normal increase in size and distribution of a population. For instance, Bromus tectorum
was introduced to intermountain western North America around 1890, and remained in localized populations for 20 years. This lag phase was followed by 20 years of logistic range expansion; by 1930 B. tectorum
was dominant over 200,000
Crooks and Soule (12) note that in addition to the normal population growth lag phase there are other mechanisms that can keep newly introduced species at low levels for decades before they become invasive. These include environmental change, both biotic and abiotic, after establishment and genetic changes to the founder populations that enable subsequent spread. Evidence for the former cases is abundant but scarce for the latter.
In summary, the biotic background for evolution has been changing since the Age of Exploration, and at an ever-accelerating pace because of accumulative effects of the numbers of species involved, the increased rate of exchange, and the lag debts that communities have amassed.
Looking to the Past. There are examples from the past of sudden mixing of biotas that were formerly isolated; one of these is fairly recent and instructive. The biota from the Red Sea and the Mediterranean Sea were reconnected, after a separation of millions of years, by the construction of the Suez Canal in 1869. The pathway for movement between these water bodies has changed since 1869 because of the varying salinity of a lake in the canal system; that is, there has not been totally free exchange without barriers. Nonetheless, over 250 species, 34 new genera, and 13 new families have moved into the Mediterranean Sea from the Red Sea, yet there has only been one documented extinction (13). These invasions have primarily been accommodated by niche displacements through competitive interactions among the congeners (14). Many of the native fish in the Mediterranean have maintained their preinvasion feeding habits but have been displaced in depth by the Red Sea invaders, which prefer the shallower, warmer, waters at the surface (15). Two nocturnally foraging fish (Sargocentron rubrum and Pmpheris vanicolensis) have shown large population increases after invading the Mediterranean from the Red Sea. Night foraging is an uncommon strategy among native Mediterranean fish (only one feeds at night), hence these migrants were probably successful because this novel behavior allowed them to exploit resources that the native fauna had not yet used.
There have been a number of spectacular population explosions of the Red Sea immigrants through time, most of which have eventually become reduced in size (14
). An exception is Rhopilema nomadica
, a large Red Sea jellyfish that experiences population explosions and crashes each summer off the coast of Israel.
The Great American Interchange of biota, the result of the isthmian land bridge that formed during the Late Pliocene, provides further information on the consequences of the mixing of previously isolated biota. However, the course of temporal resolution of the information available does not make it possible to say with certainty whether the losses of biota that occurred subsequent to the bridge were due to competition with new arrivals, although it appears likely (16). The effects of the interchange apparently were asymmetrical, with the immigrants from the south "insinuating" into the northern biota, whereas the northern immigrants to the south may have caused extinctions and undergone subsequent evolutionary radiation (17).
What we lack is detailed information on the impacts of the exchanges of biota on time frames greater than centuries but less than millions of years. In the century time frames we have processes that are still in a state of flux at the community level and ones that have been that have not been studied in detail. In the geological time frame, the poor temporal resolution does not permit us to clearly understand the mechanisms that have led to what we see in the fossil record.