Chapter 9 Biological Invasions and The

CHAPTER 9

Biological Invasions and the Homogenization of Faunas and Floras

Julian D. Olden 1 , Julie L. Lockwood 2 , and Catherine L. Parr 3

1School of Aquatic and Fishery Sciences, University of Washington, Seattle, USA 2Ecology, Evolution, and Natural Resources, Rutgers University, New Brunswick, NJ, USA 3Environmental Change Institute, School of Geography and the Environment, University of Oxford, Oxford, UK

9.1 THE BIOGEOGRAPHY OF however, the large majority of species are not distrib- SPECIES INVASIONS uted broadly, because individuals of most species have limited dispersal capabilities. In considering the distribution of organic beings These limitations on dispersal ability have produced over the face of the globe, the ﬁ rst great fact which the interesting phenomenon that many, perhaps even strikes us is, that neither the similarity nor the dis- most, species do not occupy all of the areas of the world similarity of the inhabitants of various regions can in which they could quite happily thrive. Instead, they be accounted for by their climatal and other physical are restricted to certain regions, where they are able to conditions … A second great fact which strikes us in interact with only those species with which they co - our general review is, that barriers of any kind, or occur. The limited geography of species is responsible, obstacles to free migration, are related in a close and in part, for the fantastic array of diversity that presently important manner to differences between the pro- carpets the Earth, as it provides opportunity for con- ductions of various regions. vergent evolution in disparate unconnected regions. (Charles Darwin, 1859 , pp. 395 – 396) With the range expansion of modern humans, initially out of Africa, then across the globe, came the possibility of human - mediated dispersal of a large 9.1.1 The i nvasion p rocess variety of other species. By this, we mean that humans provided the conduit for individuals of some species to One of the fundamental elements of life on Earth is disperse much farther abroad than they could natu- change. Species appear through time via evolution and rally. Species were moved within, or on, humans as disappear by the natural actions of environmental parasites or disease organisms, in their household change (e.g. volcanic eruptions, changing sea levels, goods as hitchhikers, as their livestock or working glaciation). Species have also regularly shifted their animals, as their crop plants, as their pets, and as com- geographical ranges in response to biological and phys- modities themselves. ical forces, sometimes becoming less common and There is written evidence that intentional move- other times becoming more widespread. In general, ments of species by humans traces back to ancient

Conservation Biogeography, First edition. Edited by Richard J. Ladle and Robert J. Whittaker. © 2011 by Blackwell Publishing Ltd. Published 2011 by Blackwell Publishing Ltd. Conservation planning in a changing world 225 times, such as the introduction of the tamarind tree ( Tamarindus indica ) into China by way of commerce along the Shu - Yan trade route that linked China to India 8,000 years ago (Yan et al. , 2001 ). Some species apparently have nearly circumglobal distributions because of ancient trade activities, with many of these examples only recently coming to light thanks to the power of molecular analyses to locate the evolutionary origins of now very widespread species (e.g. Wares et al ., 2002 ). There is ample historical evidence that the number of species that were moved out of their native ranges and introduced to somewhere novel via human actions increased as the world began to become ever more interconnected (Elton, 1958 ). As this number grew, the need to understand how this process occurs, and to differentiate natural species ’ range expansions from those mediated by humans, became critical. Without making this distinction, it becomes diffi cult to untangle the mechanisms that are driving historical biodiversity changes, to understand the role of new arrivals in driving evolutionary dynamics and, more practically, to stem the fl ow of species that cause ecological or economic harm (see below). Before continuing, however, it is very important to recognize that a multitude of names have been given to species that are introduced to a novel location via human actions – such as ‘ exotic ’ , ‘ invasive ’ or ‘ alien ’ species (Lockwood et al., 2007 ). We use the term ‘ invasion ’ to refer to the process whereby species expand their geographical distribution outside of their natural Figure 9.1 Generalized stages common to all species dispersal range via the actions of humans, while we invasions. A species must successfully transition through refer to populations that have become otherwise estab- each sequential stage, and the proportion of species that lished outside the bounds of their native ranges as proceed from one stage to the next is less than the previous ‘ non - native ’ . one (depicted by arrow width). A more lucid understanding of the invasion process may be achieved if it is considered as a stepwise pro- ranges and become pests. These estimates were based, gression of events, whereby individuals of some species in large part, on non - native animals and plants of are moved out of their native ranges, released into a Britain. More recently, Jeschke and Strayer (2005) novel location, establish self - sustaining populations investigated all freshwater fi sh, mammal and bird there and then spread to new locations (Figure 9.1 ; species native to Europe or North America that have Sakai et al. , 2001 ). been introduced outside their native range. They found Fundamental to this process is that not all individu- that the frequencies of transitions across all three of als successfully pass through all these stages. The tens the above stages averaged 6.1 per cent, 56.0 per cent rule of Williamson (1996) states that only ≈ 10 per and 59.7 per cent, respectively. cent of transported individuals are released into a Regardless of the specifi c percentages for each stage, foreign location, ≈10 per cent of these introduced it is apparent that only a fraction of the species that are species will go on to survive and successfully breed (i.e. moved by people, either on purpose or by accident, will establish a new population) and ≈ 10 per cent of these complete all stages of the invasion process. A consider- established species will expand their geographical able amount of research within invasion biology has 226 Biological invasions and the homogenization of faunas and fl oras therefore focused on attempts to understand which show a much wider array of biological traits than factors differentiate between those species that suc- those species that are likely to experience natural long- cessfully progress through all invasion stages and those distance dispersal. that do not (Lockwood et al. , 2007 ). The rate at which non - native populations are establishing around the world is consistently several orders of magnitude larger than fossil- derived estimates for 9.1.2 Human - a ssisted v ersus natural dispersal events at the same locations. For p rehistoric i nvasions example, the invasion rate of terrestrial species for the Hawaiian Islands was approximately 30 species per A valid and persistent question is the extent to which million years (0.00003 per year) prior to human set- modern trends in species invasions differ from those tlement, but increased to 20,000 species per million that occur naturally. This question is especially rele- years (0.02 per year) after the arrival of the Polynesians vant to students of biogeography because range expan- and to approximately 20 per year during the past two sions are a very clear component of palaeoecological centuries (Ricciardi, 2007 ). In other words, contempo- and historical biodiversity patterns (Vermeij, 2005 ). rary rates of biological invasions are nearly one million Do modern invasions warrant the attention currently times higher than the prehistoric rate for Hawaii before given to them by scientists? How different are the human infl uence. mechanisms, spatial patterns and rates of modern The number of individuals of each species being versus prehistoric invasions? Can we use prehistoric transported is also vastly different between natural and trends to help predict the consequences of modern bio- human - assisted invasion events. Natural dispersal logical invasions? events typically involve a few individuals of a species Human - assisted dispersal of non - native species fi nding their way out of the native range and attempt- differs from natural dispersal events in several impor- ing to establish a self- sustaining population in the tant aspects (J.R.U. Wilson et al. , 2009 ). Ricciardi novel locale. Occasionally the number of individuals in (2007) detailed the differences between prehistoric these natural events can be quite high – as for instance, and human- assisted invasions, which we summarize during biotic interchanges involving episodic events of below and in Table 9.1 . mass dispersal. For example, the opening of the trans- The most obvious differences are in the number polar corridor between the Pacifi c and Atlantic oceans and frequency of ‘ dispersal ’ events. Natural dispersal and the formation of the Panamanian land bridge events are characteristically rare, both in the number between North and South America during the Great of species being transported and in the temporal fre- American Interchange permitted a massive fl ux of quency with which species disperse. By contrast, species between formerly isolated regions (Vermeij, modern human- assisted dispersal events happen con- 2005 ; Lomolino et al. , 2006 ). By contrast, human - stantly and involve a wide variety of species, which assisted dispersal events are commonly characterized

Table 9.1 A comparison of key characteristics of prehistoric versus human- assisted invasions. Modiﬁ ed from Table 1 of Ricciardi (2007) .

Characteristics Prehistoric invasions Human - assisted invasions

Frequency of long- distance dispersal event Very low Very high Number of species transported per event Low* High Propagule size per event Small* Potentially large Number of mechanisms and routes of dispersal Low High Temporal and spatial scales of mass transport events Episodic (short - distance) Continuous (long- distance) Degree of homogenizing effect Regional Global Potential for interactions with other stressors Low Very high

* Except during biotic interchange events. Conservation planning in a changing world 227 by the release of hundreds to thousands of individuals 9.1.3 Economic and e cological i mpacts of a species into one novel locale, although there is of i nvasion much variation around this number. Finally, human- assisted invasions serve to connect The interest in human- assisted invasions has grown two or more locations that are geographically very rapidly over the past two decades, which is attributable distant from one another, whereas natural dispersal to three factors (Lockwood et al. , 2007 ): events tend to link sites that are comparatively close • First, as the world economy globalizes, there are together or otherwise linked naturally. Quite simply, increased trade and social connections between geo- patterns of modern dispersal unite parts of the world graphical localities, and along with these connections solely by social and economic ties, as opposed to bio- come the introduction of non- native species (Perrings physical pathways such as prevailing wind directions, et al. , 2005 ; Hulme, 2009 ). Thus, the sheer number of jet streams or ocean currents, as would happen for non - native populations establishing worldwide has natural dispersal events (Box 9.1 ). increased substantially in recent times.

Box 9.1 The h uman i mprint on m odern d ay s pecies d ispersal p atterns

The Earth is now better connected via human transport than ever before. In recent decades, human activities have greatly increased the frequency and spatial extent of species introductions across the globe through both intentional and unintentional actions. These include ballast - water discharge from international shipping; bait- bucket releases associated with recreational ﬁ shing; the global pet trade; intentional translocations of wildlife for recreation purposes; biological control; and inadvertent releases from aquaculture and horticulture activities. The following two case studies illustrate how modern biotas are connected via social and economic networks and by sea and air.

Ship t raffi c In marine and estuarine systems, the dominant invasion pathway worldwide is the ballast water of commercial ships (Carlton & Geller, 1993 ; Drake & Lodge, 2004 ). Ocean - going vessels must achieve proper stability to minimize drag (and thus maximize speed) and to reduce the likelihood of capsizing in rough seas. To achieve this, early ships strategically fi lled ballast compartments within the hull with soil, rocks or scrap metal – essentially, anything with some weight that could be easily loaded into a ship at dock. Today, ships pump water into ballast tanks, and a typical commercial bulk vessel might carry over 30,000 metric tonnes of ballast water during an inter - oceanic voyage. Ballast water is usually taken from the harbour in one port and subsequently may be discharged in a recipient port through openings in the ship ’ s hull. The number of non- native species that are transported via ship ballast has increased with the rise in global commerce and the consequent upsurge in the number of ships travelling the world ’ s oceans and major waterways (Figure B9.1a ). Current estimates suggest that a global fl eet of approximately 35,000 commercial vessels transports an annual volume of about 3.5 × 10 9 metric tonnes of ballast water, containing some 7,000 – 10,000 species (mostly marine) at any one time (Wonham et al., 2005 ). Even if only a small fraction of these species establish non- native populations, it is easy to see that ballast water is a primary mechanism by which aquatic invasions are occurring. By tracking the number of ships that visit ports worldwide, Drake and Lodge (2004) were able to map ‘ hotspots ’ of marine invasions and, via network modelling, to determine which ports are likely to have increased rates of invasions in the coming years (Figure B9.1a ). These hotspots are clearly the product of economic and social infl uences on global trade and are in marked contrast to what we might expect given natural dispersal patterns of marine species via oceanic currents. 228 Biological invasions and the homogenization of faunas and fl oras

Figure B9.1a (a) The frequency of commercial shipping trafﬁ c along shipping routes around the world, ranging from low (blue) to high (red). From Halpern et al. (2008) . (b) Global hotspots for biological invasion from ballast water, ranging from low (blue) to high (red). From Drake and Lodge (2004) . (See Plate B9.1a for a colour version of these images.)

Airline t raffi c International air travel has been recently pinpointed as a signifi cant factor in the movement of economically damaging pest species and infectious diseases (Tatem, 2009 ). Among others, the Mediterranean fruit fl y Ceratitis capitata has been consistently imported in airline baggage (Liebhold et al., 2006 ), plant pathogens are often found in air cargo (McCullough et al., 2006 ) and disease - carrying mosquitoes have survived long haul fl ights in aircraft cabins (Lounibos, 2002 ). Far - removed regions with similar climates have now been suddenly linked by a busy fl ight schedule, which has resulted in an elevated risk of foreign invasions. This risk, however, depends greatly on the time of year. Tatem and Hay (2007) identifi ed an ‘ invasion window’ across the global air network from June to August, when climatic conditions in regions linked by long - haul routes are most similar to one another and the higher number of fl ights increases the chances of exotic species hitching a ride to somewhere new. With expected increases in global trade and travel (Perrings et al., 2005 ; Hulme, 2009 ), opportunities for such extreme hitchhiking through the world airline transportation and shipping network look set to increase further (see trend in Figure B9.1b ).

Figure B9.1b Trends in global shipping cargo volumes and air freight, 1970– 2005. From Hulme (2009) . Conservation planning in a changing world 229

• Second, as the number of non - native populations of which is the widespread distribution of Norway rats increases, scientists fi nd it increasingly hard to ignore ( Rattus norvegicus). This rodent species was regularly, them. It is important to recognize that many of these and inadvertently, transported with human colonists species present unique opportunities to test various as they expanded across the globe. They serve as the ecological, evolutionary and biogeographical concepts reservoir and vector for a variety of particularly trou- and theories. Certainly the basic insights gained from blesome human diseases, the most well know being the study of modern invasion events are substantial bubonic plague. (Sax et al. , 2007 ). In general, scientists reserve the term ‘ invasive ’ for • Third, some of the non - native populations that have these few non- native species that cause ecological or established have gone on to impart substantial eco- economic harm. It is an open question as to whether nomic and ecological cost (Simberloff et al. , 2005 ; these few invasive species have characteristics that Pimentel et al. , 2006 ). make them unique amongst the world’ s species, but As detailed above and shown in Figure 9.1 , not all there is a clear need to be able to identify them as species that are dispersed via human actions have potentially harmful long before they have the chance negative impacts within their new environment. The to become invasive. defi nition of what constituents ‘ impact ’ is somewhat problematic for at least two reasons: 1 There are scientifi c and societal infl uences on the 9.2 BIOTIC HOMOGENIZATION perception of impact (not to mention that the effects of invasive species are often subtle and diffi cult to observe). The regional connectivity of the world is stronger and 2 After impact is perceived, there is a variety of eco- more varied than ever before and, consequently, there logical factors that determine the level of impact pro- are very few places where non- native species have not duced (Lockwood et al. , 2007 ). become established. Looking back over human history, Let us move past this issue by simply conceding that it is apparent that changes in species diversity are human perception and valuation are an integral part frequently the result of the widespread invasion of of the integration stage of the invasion process (Figure ubiquitous non- native species into areas containing 9.1 ). It is important to recognize that the proportion of rare, and often unique, native species (Elton, 1958 , species that do cause harm as compared to those that Ricciardi, 2007 ). are simply moved out of their native range is quite low. If the same non- native species are being introduced Nevertheless, these few species will eat, parasitize and to multiple locations, then there is potential for dis- compete with native species, often driving the latter parate regions to become more similar in their species extinct or into very low population numbers (Elton, composition through time, a process known as biotic 1958 ; Clavero & Garc í a - Berthou, 2005 ; Strayer et al. , homogenization. There are certainly well - known 2006 ). Some non- native populations invade natural invaders that can be found nearly everywhere. These areas such as parks or wildlife reserves and disrupt days, for example, you can land at nearly any airport native species communities (Simberloff et al. , 2005 ). In in the world and, while waiting for your next fl ight, these instances, the value of the natural area in terms watch house sparrows (Passer domesticus) cavorting on of its ability to conserve biodiversity may be reduced if the tarmac. This species is native to Eurasia, but it has the non- native is not controlled or eradicated. realized a very broad geographical distribution via Many species threaten human economic interests, human - mediated introductions. notable examples including the zebra mussels ( Dreissena For many years, the biodiversity crisis has been polymorpha) that clog utility companies’ water intake focused on the loss of species through global extinc- valves (MacIsaac, 1996 ); emerald ash borers (Agrilus tion. Although this is clearly of prime importance, at planipennis ) that devastate urban and commercial sub- global scales the loss of populations through local forests (Poland & McCollough, 2006 ); and monk para- extirpation, combined with the invasion of already keets (Myiopsitta monachus ), whose bulky nests can common non - native species, may be the more dra- cause electric power line failures (Avery et al. , 2002 ). matic reconfi guration of modern biodiversity. In fact, A substantial number of non- native species have changes in diversity patterns at fi ne and coarse scales adverse impacts on human health by transmitting dis- of analysis can be either concordant or, alternatively, eases (Lounibos, 2002 ; Tatem, 2009 ), the most obvious can be decoupled and even confl icting. 230 Biological invasions and the homogenization of faunas and fl oras

For example, Pautasso (2007) conducted a meta - diversity across a study region, a phenomenon termed analysis of the relationship between human popula- ‘ biotic differentiation ’ by Olden and Poff (2003) . tion size and change in the plant and animal species richness of study areas. The study reported negative changes in richness at small spatial scales of analysis 9.2.1 The p rocess of b iotic h omogenization (or small extent) but positive changes at larger spatial scales. The introduction of non - native species by In the simplest sense, human activities that increase humans is typically integral to such changes. In rates of species invasions and extirpations are the ulti- essence, anthropogenic changes driving habitat loss, mate cause of biotic homogenization. However, biotic fragmentation, species invasions and ecosystem trans- homogenization can arise when only invasions occur formation may result in declining local richness but, without the concurrent loss of species, or conversely across larger landscapes and regions, relatively few where only species extirpations occur. In other words, native species may become entirely extinct, while non- species additions or replacements need not occur for natives boost the richness above natural baseline levels. regions to become homogenized or even differentiated Changes such as these, in the inventory richness of over time (Olden & Poff, 2003 ). smaller areas nested within larger regions, may also be To illustrate this point, we provide a simple graphical accompanied by changing patterns in differentiation example showing how the number and manner in diversity, i.e. in the degree of compositional turnover which non - native species establishment and native between localities – also known as ‘ beta diversity ’. A species extirpations occur may lead to very different change in beta diversity can, in fact, occur either levels of homogenization or differentiation (Figure through a reduction in the total number of species in 9.2 ). In the absence of any extirpation, the establish- the region (regional species richness or sometimes ment of the same non - native species at two separate ‘ epsilon diversity ’ ) or through a change in the species localities will lead to increases in the similarity of the similarity between areas. Basically, if a similar suite of invaded communities. Conversely, the establishment of species is shared across the areas in a region, beta a different non - native species at each locality will diversity will be quite low. If very different species decrease community similarity. Although this example occur in different areas, beta diversity will be high. is useful to illustrate the simplest way biotic homogeni- Biotic homogenization is thus a term describing the zation can occur, both empirical data and theoretical process of reducing differentiation diversity between modelling suggests that the process is both complex regions, but it may be accompanied by varying and sensitive to the spatial and temporal scale of inves- patterns of change in inventory richness at different tigation (Olden, 2006 ). scales of analysis. See Box 1.2 for an explanation of terminology. Put another way, biotic homogenization is described 9.2.2 Different m anifestations of b iotic as the process by which regionally distinct native com- h omogenization munities are gradually replaced by locally expanding, cosmopolitan, non - native communities (McKinney & Biotic homogenization is considered an overarching Lockwood, 1999 ). Some have likened the process of process that encompasses either the loss of taxonomic, biotic homogenization to the now global distribution of genetic or functional distinctiveness over time (Olden fast - food restaurants, coffee houses and big - box retail- et al. , 2004 ). Taxonomic homogenization, which we ers (Olden et al., 2005 ). The more connected we are as used to introduce the concept of homogenization a society, the more likely we are to see the trans - global above, has been the primary focus of previous research distribution of both species and businesses. In circum- and is commonly referred to as biotic homogenization. stances where invasive species impact negatively on However, imposing a narrow deﬁ nition of biotic homo- locally co- occurring native species, rare and endemic genization does not truly reﬂ ect the multidimensional native species may be lost, resulting in rapid loss of nature of this process. Consequently, it is useful to differentiation diversity. However, it is also important think of biotic homogenization as a broader ecological to recognize that the reverse can also occur and that, process by which formerly disparate biotas lose biologi- in cases, the combined effects of invasions and extirpa- cal distinctiveness at any level of organization, includ- tions can be to increase the mean differentiation ing in their genetic and functional characteristics. Conservation planning in a changing world 231

Figure 9.2 Illustration of how species invasions and extinctions can cause either biotic (taxonomic) homogenization in scenario 1 or differentiation in scenario 2, depending on the identity of the species involved. A pair of communities (shaded ovals) for each scenario is illustrated, where extirpation events are represented by the disappearance of a species icon over a time step, whereas introduction events are represented by the arrow and appearance of a species icon. Importantly, both scenarios share the same species pool (6 native butterﬂ ies, 2 introduced butterﬂ ies) and species richness through time is identical for both scenarios. From Olden and Rooney (2006) .

Let us spend a moment exploring these two additional • First, the intentional translocation of populations ways in which biotic homogenization can be from one part of the range to another enhances the manifested. potential for intraspeciﬁ c hybridization (i.e. hybridiza- Genetic homogenization refers to a reduction in tion between different sub- species within a species), genetic variability within a species or among popula- with the end result being the assimilation of gene pools tions of a species. It can occur through at least three that were previously differentiated in space (Stockwell mechanisms: et al. , 1996 ). 232 Biological invasions and the homogenization of faunas and ﬂ oras

• Second, introductions of species outside of their Although the jury is still out on this, it is clear that the original range(s) increases the likelihood of a founder study of biotic homogenization represents a unique effect and reduced levels of genetic variability, as well challenge because it is a multifaceted process, encom- as setting the stage for interspecifi c hybridization (i.e. passing both species invasions and extirpations, which hybridization between different species within the requires the explicit consideration of how the identities same genus) (Rhymer & Simberloff, 1996 ). of species (not just species richness) change over both • Third, if extirpations were a cause for faunal homog- space and time. enization, then one consequence might be bottleneck(s) A simple perusal of the literature shows that the in local populations of the impacted species, along with majority of research to date has focused on quantifying lowered effective population size(s) (Lee, 2002 ). patterns of taxonomic homogenization, whereas the Functional homogenization refers to an increase in processes of genetic and functional homogenization the functional similarity of biotas over time resulting have received considerably less attention. Moreover, from the replacement of ecological specialists by the even estimates of taxonomic homogenization are same widespread generalists. It occurs primarily sparse and highly variable within and between taxo- because patterns of species invasions and extirpations nomic groups. Despite this trend, tremendous progress are not random, but instead are related to particular has been made in recent years to better understand biological traits that commonly predispose native and quantify patterns of taxonomic homogenization species to extirpation and non- native species to suc- (Table 9.2 ). We review the taxonomic groups (fi shes, cessful establishment. The end result is an increase in birds, plants and mammals) that have received the the functional convergence of biotas over time associ- most attention next. ated with the establishment of species with similar ‘ roles ’ in the ecosystem (e.g. high redundancy of functional forms or traits) and the loss of species possessing 9.3.1 Fishes unique functional ‘ roles ’ (McKinney & Lockwood, 1999 ; Olden et al. , 2004 ). The homogenization of freshwater fi sh faunas has For example, Winter et al. (2008) examined how the received the greatest attention thus far. In a landmark presence of non - native plant species in Germany study, Rahel (2000) compared the species similarity of affected the distribution of a genetic trait, namely US states between present - day and pre - European set- ploidy level (referring to the number of homologous tlement time frames and found that pairs of states aver- sets of chromosomes in a biological cell), at two spatial aged 15.4 more species in common now than they did scales. It is commonly accepted that polyploidy species in the past. On average, fi sh faunas became more should have a greater ability to colonize or invade new similar by 7.2 per cent, with the highest increases in habitats due to greater genetic variability. Interestingly, similarity observed in western and north- eastern states this study found evidence for functional differentiation (Figure 9.3 a). The high degree of biotic homogeniza- at fi ne spatial scales ( < 130 km 2) due to more heteroge- tion is best illustrated by the fact that the 89 pairs of neous ploidy levels of non - native plants compared to states that historically had zero similarity (no species native plants, whereas, at a coarser spatial scale, more in common) now share an average of 25.2 species, homogeneous ploidy levels of non- native species lead resulting in an average present- day similarity of 12.2 to functional homogenization. per cent. Patterns of fi sh homogenization were primarily the result of non- native species establishment associated with fi sh stocking for recreational purposes (e.g. 9.3 PATTERNS OF BIOTIC brown trout (Salmo trutta ), rainbow trout (Oncorhynchus HOMOGENIZATION mykiss) and smallmouth bass ( Micropterus dolomieu ) or aquaculture (e.g. common carp, Cyprinus carpio ), and Many scientists, including ourselves, have argued that to a smaller degree the extirpation of endemic species we are entering a period characterized by widespread (harelip sucker, Lagochila lacera ). faunal and fl oral homogenization, fi ttingly dubbed the Taylor (2004) found a similar pattern among ‘ Homogecene ’ , in a place appropriately called the ‘ New Canadian provinces and territories, where average Pangaea’ (the original Pangaea being the global super- faunal similarity increased from 27.8 per cent to 29.1 continent of approximately 250 million years ago). per cent – a trend driven in large part by the differential Conservation planning in a changing world 233

Table 9.2 Review of the published studies that report estimates of community similarity change between two time periods in the context of biotic (taxonomic) homogenization. Change in similarity refers to mean pair- wise difference between historical and extant community similarity across all sites, unless otherwise noted. Positive values indicate homogenization and negative values indicate differentiation. Note that this table only includes studies for which estimates of per cent change in community composition were reported.

Taxonomic group Change in Location Spatial extent Unit similarity Reference

Freshwater ﬁ shes Australia Country - wide Basin divisions 3.0% Olden et al. (2008) 3 North - eastern Coastal watersheds − 1.4% coastal

Canada Country - wide Provinces/territories 1.3% Taylor (2004) 1 British Columbia Aquatic ecoregions − 3.5%

Europe Country - wide Major basins 2.2% Leprieur et al. (2008) 1 Iberian Peninsula Major basins 17.1% Clavero & Garcí a - Berthou and France (2006)1

USA Country - wide States 7.2% Rahel (2000) 1 California Zoogeographic 20.3% Marchetti et al. (2001) 1 provinces Watersheds − 10.7% South Dakota Geomorphic provinces 8.0% Hoagstrom et al. (2007) 1 Watersheds 2.4% Minnesota Lakes 9.0% Radomski & Goeman (1995) 1 Kansas Streams − 0.2% Eberle & Channell (2006) 1

Amphibians and reptiles USA Florida Select counties − 0.8% Smith (2006) 1

Terrestrial plants Canada & USA Country - wide States and provinces 1.2% Qian & Ricklefs (2006) 1

Canada & USA Select regions States and provinces − 0.6% Rejm á nek (2000) 1

Chile Country - wide Administrative regions 0.3% Castro & Jaksic (2008) 1,7 South - eastern Islands 2.0% Castro et al. (2007) 1 Paciﬁ c

Europe Germany Grid cells (130 km 2 ) 3.9% K ü hn & Klotz (2006) 5

Europe & USA Select regions Forest stands 3.9% Vellend et al. (2006) 6

Great Britain Country - wide Grid cells (1 km 2 ) − 1.0% Smart et al. (2006)1

United States Select regions Parks and local areas 0.8% McKinney (2004) 1 Countries 0.5% Schwartz et al. (2006) 3 Wisconsin Forest stands 2.6% Rooney et al. (2004) 2 234 Biological invasions and the homogenization of faunas and ﬂ oras

Table 9.2 Continued

Taxonomic group Change in Location Spatial extent Unit similarity Reference

Terrestrial birds Canada & USA Country - wide Transects − 2.0% La Sorte & Boecklen (2005) 4

Netherlands Country - wide Grid cells (5 km) 2.8% Van Turnhout et al. (2007)2

Global Atlantic Ocean Oceanic Islands 0.9% Cassey et al. (2007) 3 Caribbean Ocean − 0.9% Indian Oceans 1.8% Paciﬁ c Ocean − 0.2%

Terrestrial mammals Global Select countries Country 2.1% Spear & Chown (2008) 1 South Africa Country - wide Grid cells (0.25 degree) − 1.3% Grid cells (1 degree) 4.2% Grid cells (2 degrees) 8.1%

Taxonomic similarity based on: 1 Jaccard ’ s Similarity Index, 2 Bray - Curtis Similarity Index, 3 S ö rensen ’ s Similarity Index, 4 Beta - sim Index, 5 Simpson ’ s Index, 6 Raup and Crick Index of beta diversity, 7 Mean values based on a published range.

invasion of 48 non- native fi shes over the past century contrasting effects on the changes in community simi- (Figure 9.3 a). larity (Leprieur et al. , 2008 ). Although biological inva- Similar broad- scale efforts have been conducted in sions have resulted in an overall increase in faunal other parts of the world. Recent evidence points to the similarity on the order of 2.2 per cent (Figure 9.4 a), homogenization of Australian fi sh faunas in response this research found that translocated native species (i.e. to human- mediated species introductions (Olden et al. , species introduced by humans into regions where they 2008 ). Fish compositional similarity among major were not historically found) promoted homogenization drainages increased 3.0 per cent, from a historical among basins (+ 5.0 per cent: Figure 9.4 b), whereas similarity of 17.1 per cent to a present- day similarity exotic species (i.e. species originating from outside of 20.1 per cent. Sometimes, the degree of faunal Europe) tended to decrease their compositional similar- similarity between drainages doubled or even tripled ity ( − 1.6 per cent: Figure 9.4 c). This fi nding is highly with time. This trend was particularly obvious in the consistent with patterns in fl oral homogenization (dis- southern corners of the continent – areas which are cussed in Section 9.3.3 ), suggesting that differences in highly populated relative to other regions of Australia the geographical distribution of exotic and translo- (Figure 9.3 b). Similar to the United States and cated species may play an important role in shaping Canada, fi sh faunal homogenization in Australia was patterns of homogenization. the result of the widespread introduction and subse- Clavero and Garc í a - Berthou (2006) used distribu- quent escape/spread of non- native fi shes for recreation tional data for freshwater fi sh in four time periods to (rainbow trout), aquaculture (common carp) and mos- assess the temporal dynamics of biotic homogenization quito control (western mosquito fi sh, Gambusia affi nis ), among river basins in the Iberian Peninsula. They and from the ornamental/aquarium trade (goldfi sh, found strong evidence for biotic homogenization, with Carassius auratus; guppy, Poecilia reticulata ). faunal similarity among rivers basins increasing by Recent efforts in Europe have shown that exotic and 17.1 per cent from historical times to the present day. translocated native species generate distinct geograph- Changes in faunal similarity were highly dynamic in ical patterns of biotic homogenization because of their time. The establishment of non - native species in 1995 Conservation planning in a changing world 235

Figure 9.3 Fish faunal homogenization of: (a) states and provinces in the United States and Canada (data from Rahel (2000) and Taylor (2004) , respectively); (b) major drainage divisions of Australia (from Figure 2 of Olden et al. , 2008 ). resulted in slight differentiation, but by 2001 the range regions exhibited a 2.8 per cent increase in community expansion of previously established non- native species similarity. Signifi cant spatial variation in patterns of caused biotic homogenization in some regions and the homogenization existed. Low- lying western regions continuing addition of new non - native species led to exhibiting low historical species richness showed the biotic differentiation in others. greatest increase in resemblance by converging towards those avifaunas more characteristic of eastern regions. Based on breeding bird surveys for North America 9.3.2 Birds (exclusive of Mexico), La Sorte and Boecklen (2005) showed substantial change in the diversity structure Avifaunal homogenization has been another area of of avian assemblages at the local scale in non - urban recent focus, although the number of studies are areas from 1968 to 2003. However, there was little limited compared to fi shes. In the Netherlands, Van evidence that overall similarity in species composition Turnhout et al. (2007) evaluated changes in breeding was increasing – in fact, the general trend was towards bird composition over a 25- year period and found that a two per cent level of biotic differentiation. Despite 236 Biological invasions and the homogenization of faunas and fl oras

Figure 9.4 Fish faunal homogenization of major river drainages in Europe based on: (a) all non - native species; (b) only translocated native species; (c) only non- native species originating from outside Europe. Adapted from Figure 1 of Leprieur et al. (2008) . this, their study did fi nd that more highly populated among archipelagos but, in general, avian assemblages regions located closer to the Atlantic and the Pacifi c tended to show increased similarity over time to other coasts of the United States experienced the strongest islands within their archipelago, compared with islands patterns of homogenization. outside their archipelago. Islands in the Indian Ocean At the global scale, Cassey et al . (2007) explored pat- exhibited the greatest homogenization, whereas biotic terns of invasion and extirpation and their infl uence differentiation occurred for most islands in the Atlantic on the similarity of oceanic island bird assemblages Ocean. However, although avifaunal homogenization from the Atlantic, the Caribbean, and the Indian and was apparently the rule rather than the exception for Pacifi c Oceans. The authors found that patterns of islands in the Indian Ocean, the authors found that the homogenization differed signifi cantly between and relationship of this change to initial similarity was Conservation planning in a changing world 237 scale- dependent. At smaller spatial scales (islands Distributional patterns of native and non- native within archipelagos), the expected pattern of low species may vary in such a way that they will have initial similarity leading to greater homogenization opposing effects on patterns of homogenization. For was observed, whereas this relationship reversed at the example, Qian and Ricklefs (2006) evaluated changes larger spatial scale of islands between archipelagos. in differentiation diversity of vascular plants across This study illustrates that the spatial extent of inves- North America (excluding Mexico) and found that non- tigation and the evolutionary history of the region native species tended to homogenize fl oras in distant under consideration can infl uence patterns of taxo- areas whose native plant species differ greatly, but nomic homogenization and differentiation within and differentiate neighbouring areas that exhibited more across what appear to be equivalent spatial units (i.e. closely related native fl oras (Figure 9.5 ). Because few ocean basins). native species have yet been extirpated from state and provincial fl oras, these authors reason that the pattern of homogenization and differentiation probably refl ects 9.3.3 Plants the haphazard introduction and establishment of non- native species with respect to suitable habitats. At play Evidence for fl oral homogenization comes from studies is also the natural and human- assisted spread of non- conducted in many countries at a variety of spatial native species with no regard to the ecological con- scales. However, evidence to date suggests that levels straints acting on native species. of fl oral homogenization are considerably smaller than Smart et al. (2006) used botanical data for fl owering those observed for freshwater fi shes (Table 9.2 ). plants in Great Britain to test the hypothesis that plant Within the United States, McKinney (2004) found communities have become taxonomically and func- that non- native plant species contributed signifi cantly tionally more similar over the past 20 years in human- to fl oral homogenization of 20 parks and local conser- dominated landscapes. Although little evidence was vation areas, although the magnitude was relatively found for the taxonomic homogenization of plant com- low and sometimes negative (indicating differentia- munities, this study revealed that plant traits related to tion). Cosmopolitan plant species most responsible for dispersal ability and canopy height increased in their the observed homogenization included curly dock occurrence across the communities over time. The ( Rumex crispus ), dandelion ( Taraxacum offi cinale ) and authors suggest that environmental change has caused bluegrass (Poa annua ). Similarly, Schwartz et al . (2006) different plant communities to converge on a narrower found that the county fl oras of California, USA, have range of winning trait syndromes (i.e. functional shown slight homogenization. The establishment of homogenization), while species’ identities remained noxious weeds played a central role in shaping patterns relatively constant. of homogenization, but the authors suggest that the Similarly, Castro and Jaksic (2008) reported that greatest potential for future homogenization may come the compositional similarity of the continental fl ora from extirpations of extant native populations within of Chile has not shown signifi cant modifi cations counties. over time. Interestingly, this result is not shared for At a fi ner spatial scale, Rooney et al . (2004) oceanic island fl oral assemblages off the coast of Chile, re- surveyed 62 upland forest stands in northern in which present- day islands share a greater number Wisconsin, USA, to assess the degree of fl oral homog- of species compared to the pre - European condition enization of under - storey communities between 1950 (Castro et al. , 2007 ). and 2000. By incorporating changes in both species occurrence and abundance, the authors found that two- thirds of the sites had become more similar in their 9.3.4 Mammals composition as a result of declines in rare species and increases in already regionally abundant native and Interest in the process of biotic homogenization has non- native species. Interestingly, levels of homogeniza- thankfully expanded beyond fi shes, plants and birds in tion were greatest in areas without deer hunting, sug- recent years. In a compelling study, Spear and Chown gesting that selective grazing by overabundant deer (2008) examined the effects of ungulate introductions populations was acting as a key driver of fl oral on biotic similarity across four spatial scales, at three homogenization. spatial resolutions within South Africa and among 238 Biological invasions and the homogenization of faunas and fl oras

Figure 9.5 Distribution of homogenization indices ( H) among pairs of state- and province- level fl oras of the United States and Canada. The pairs of fl oras are grouped by degree of native plant similarity ( J native). Native fl oras portrayed in the left hand side panel are more distant ( Jnative = 0.00 – 0.20) than those in the middle ( Jnative = 0.20 – 0.40 and 0.40 – 0.60) and right - hand side ( J native > 0.60) panels. J total refers to fl oral similarity based on native and non- native species composition. Floral similarity is based on Jaccard’ s coeffi cient of similarity ( J), which ranges from 0 (no species in common) to 1 (all species in common). From Figure 1 of Qian and Ricklefs (2006) .

41 nations located worldwide. They found that between initially having a smaller homogenizing effect than the 1965 and 2005, ungulate assemblages had become differentiating effect of extra- regional introductions two per cent more similar for countries globally and (Figure 9.6 ). eight per cent more similar at the coarsest resolution within South Africa. Interestingly, species introduced from other conti- nents, as opposed to those introduced from within 9.4 ENVIRONMENTAL AND HUMAN Africa, were found to have different effects on patterns DRIVERS OF BIOTIC of homogenization. Homogenization was most affected HOMOGENIZATION by translocations of species from neighbouring localities (extra- limital species) (4.6 per cent increase in Environmental change ultimately promotes the geo- similarity), whereas introductions of ungulates from graphical expansion of some species and the geograph- more distant areas (extra- regional species) tended to ical reduction of others, leading to biotic homogenization differentiate assemblages (3.8 per cent decreased in (McKinney & Lockwood, 1999 ). Habitat loss, pollution, similarity). Quite simply, non - native species introduced climate change or other sources of disturbance often from distant regions are more likely to establish in only precede, and in a sense prepare, the environment for a few localities, resulting in differentiation. changes in beta diversity over time. The research high- Similar ﬁ ndings have also been reported for plants lighted above, in addition to a number of other studies and freshwater ﬁ shes in the United States (McKinney, in the literature, has provided compelling evidence 2005 ; LaSorte & McKinney, 2006 ). Levels of homo- linking human- induced environmental change to genization were found to increase with increasing biotic homogenization across taxonomic groups. resolution (see Table 9.2 ) and with time. In the South Collectively, this research has shown that human activ- African study, from 1971 to 2005, homogenization ities on the landscape are often characterized by greater by extra- limital introductions increased rapidly after increases in taxonomic similarity, suggesting that Conservation planning in a changing world 239

Figure 9.6 Temporal trends in ungulate homogenization as a result of extra- regional and extra- limital introductions in South Africa, at the quarter- degree grid cell resolution, between 1971 and 2005. Redrawn from Figure 4 of Spear and Chown (2008) .

humans are playing a central role in promoting the suggest that human settlement may directly increase homogenization process by introducing new species the likelihood of intentional or accidental non- native and favouring the persistence of non- native species species introductions, and disturbance associated with over native species. physical infrastructure and land - use change may For freshwater ecosystems, Scott and Helfman promote the establishment of these species by disrupt- (2001) reported that cosmopolitan species’ richness ing environmental conditions. increased and endemic species’ richness decreased in Wetland degradation has also led to the homogeni- response to increased watershed deforestation and zation of aquatic and invertebrate communities in density of buildings and roads in Tennessee, USA. At a Michigan, USA (Lougheed et al. , 2008 ). Specifi cally, larger spatial scale, Marchetti et al . (2001) observed habitat homogenization at both the local and land- that measures of human occupancy and aquatic scape scales were found to shift community structure habitat alteration, including the density of dams and from a species- rich and spatially heterogeneous com- aqueducts in the watershed, were associated with munity dominated by fl oating - leaved plants in unde- increased similarity of zoogeographical provinces in veloped wetlands, to nutrient- rich wetlands dominated fi sh communities in California, USA. However, at a by ubiquitous duckweed (Lemnaceae). fi ner spatial scale, Marchetti et al . (2006) found a nega- Urban/rural gradient studies have provided impor- tive relationship between change in community simi- tant insights into associations between urbanization larity and the proportion of the watershed in and bird and plant homogenization. Blair (2004) found development (including commercial, industrial, urban that temporal changes in bird community composition and suburban) – or, in other words, more developed varied in a similar fashion along an urban/rural gradi- watersheds showed greater biotic differentiation. Olden ent in the oak woodlands of northern California et al. (2008) found that geographical patterns of and the eastern broadleaf forests of Ohio, USA. The homogenization in Australia were highly concordant degree of taxonomic overlap in the bird communities with levels of disturbance associated with human increased from approximately 5 per cent in the least settlement, infrastructure and land use. These results developed sites to approximately 20 per cent in the 240 Biological invasions and the homogenization of faunas and fl oras most urbanized sites – an outcome of the replacement 9.5 BIOTIC HOMOGENIZATION AND of local endemic species (often urban - sensitive species) CONSERVATION by ubiquitous non - native species (urban - adapted species). Biotic homogenization is an important dimension of By contrast, Clergeau et al . (2006) found that avifau- the modern biodiversity crisis, with signifi cant ecologi- nal similarity of town centres in Europe was actually cal, evolutionary and social implications (McKinney & lower than in less urbanized habitats – a result that Lockwood, 1999 ; Olden et al., 2004; 2005). It extends may have been connected to the larger size of towns beyond the narrow focus on elevated extinction rates and, thus, greater types of potential habitat in this to incorporate the other side of the equation: the estab- study system. The results from this study also sug- lishment of non- native species. Biotic homogenization gested that urbanization might cause homogenization conjures the prospect of Kunstler ’ s (1993) The by decreasing the abundance of ground- nesting bird Geography of Nowhere , in which biotic distinctiveness is species and bird species that preferred bush/shrub gradually dissolving over time. Consequently, a major habitats. Schwartz et al . (2006) reported fl oristic challenge within conservation biogeography is to iden- homogenization of urbanized counties in southern tify and understand present - day patterns of biotic California, whereas they found no change in more homogenization to guide policy aimed at mitigating its rural areas of northern California. The study of Kü hn future effects (Rooney et al. , 2007 ). and Klotz (2006) , on the other hand, found no overall Clearly, the most effective conservation of biodiver- relationship between patterns of homogenization and sity involves reducing and, where possible, preventing urbanization across Germany. the two processes generating biotic homogenization – In summary, although urbanization undoubtedly species invasions and extinctions. The conundrum is plays a role in shaping patterns of biotic homogeniza- determining the best way to achieve this goal. Because tion, the exact nature and generality of this relation- the key factors facilitating homogenization include ship is still unclear (McKinney, 2006 ). people and habitat transformation (through extinc- Environmentally mediated interactions between tions or the establishment of non- native species), a fi rst species may also be an important driver of biotic step towards achieving biodiversity conservation goals homogenization. Holway and Suarez (2006) examined is to focus efforts in areas subject to human activities native ant communities in scrub and riparian habitats and to reduce human- related impacts. of mediterranean California to test the hypothesis that Unfortunately, there is a strong correlation between the invasion of Argentine ant (Linepithema humile ) has human population density and species richness, and caused biotic homogenization. By comparing invaded the areas of high biotic diversity that are under the and un - invaded sites across similar habitats, the greatest threat are often in the most populated areas authors showed that sites invaded by Argentine ants (Chown et al. , 2003 ; McDonald et al. , 2008 ). Indeed, at have lower beta diversity compared to un - invaded sites. a fi ner scale of analysis, designated conservation areas Specifi cally, functional homogenization of ant commu- may often attract people to them through perceived nities occurred via shifting community dominance to benefi ts of employment, market access and foreign aid smaller- bodied workers with lower thermal tolerance (Wittmeyer et al . 2008 ). The increased external threat and a reduced diversity of behaviours (i.e. nesting from accelerated human population growth does not habits, dispersal strategies and foraging behaviours). bode well for the native biota in these areas, which con- Because Argentine ant abundance in seasonally- dry sequently face the risk of increased homogenization. mediterranean environments is positively correlated In the past, purposeful homogenization was under- with soil moisture, the authors hypothesized that the taken within countries such as Australia and some homogenizing effects of the Argentine ant are facili- Pacifi c island territories by acclimatization societies tated by inputs of urban and agricultural water run - off within colonist human societies who, for a variety of that acts to create mesic soil conditions. This observa- reasons, wanted to surround themselves with familiar, tion supports the notion that anthropogenic modifi ca- colourful or (regarding birds) tuneful species. Even tions to the environment indirectly cause biotic today, some conservation organizations encourage the homogenization by creating opportunities for the inva- intentional movement or translocation of species, sion of the Argentine ant, as opposed to threatening which may also have the unintended consequence of the persistence of native ants directly. promoting homogenization. Conservation planning in a changing world 241

This act is a problem when species are introduced unique species over time, and neither complementarity and become established outside of their historical dis- nor the level of biotic homogenization would change, tribution, or where the genetic consequences (e.g. yet the true state of biodiversity loss will not be refl ected. interspecifi c hybridization) are not considered. For example, in parks across southern Africa there has been a trend to introduce the same suite of species 9.6 NOVEL ASSEMBLAGES across nature reserves. Fuelled by tourism and the pub- lic’ s desire to see large mammals (especially predators), Novel assemblages, sometimes referred to as novel or spotted hyena ( Crocuta crocuta ), wild dog ( Lycaon pictus ) emerging ecosystems, are communities that consist of and antelope such as roan (Hippotragus equinus ) have extant species which have not occurred previously in been introduced and have established within areas the same combinations found today (Hobbs et al. , where they did not historically occur, or to areas that 2006 ). Increased homogenization of biotas associated are now unsuitable due to small park sizes. with the massive and accelerating movement of species In fact, Spear and Chown (2008) demonstrated that within and between regions/provinces is likely to con- it is extra- limital introductions that are driving the tribute substantially to the creation of novel or no - homogenization of ungulate assemblages in South analogue assemblages. Africa (Figure 9.6 ). They warn that the potential for Although, technically, any area that has lost native changes in local diversity and ecosystem functioning as species or gained non- native species is novel in some a consequence of translocations should not be under- respect, some current assemblages have been trans- estimated. These concerns contrast with other conser- formed to such an extent that they are verging on vation actors arguing for various forms of rewilding, or becoming entirely new assemblages (Williams & for assisted migrations of species as a climate- change Jackson, 2007 ). Certainly, in terms of system function- mitigation strategy (see, e.g. Chapter 3 ; Donlan, 2007 ). ing, many ecosystems have already become ‘ novel ’ . The concept of biotic homogenization and differen- One of the best examples comes from the San tiation may provide a useful tool in conservation Francisco Bay, California, which has the dubious dis- planning (Rooney et al. , 2007 ). Much attention in con- tinction of being the most invaded aquatic region on servation has focused on reserve selection and choos- Earth, with more than half its fi sh and most of its ing the best network of reserves to maximize bottom - dwelling organisms representing non - native biodiversity coverage. Such efforts have largely focused species (Cohen & Carlton, 1998 ). The total dominance on species number, endemism and complementarity as (number of species and biomass) of non- native species the metrics that should be optimized (Chapters 6 and has transformed the bay from a pelagic (mid- water) 7 ; Pressey et al. , 1993 ). system to a benthic (bottom) one and productivity has Complementarity exists when an area has some bio- declined. Invasive species such as Corbula amurensis diversity components that are unrepresented in other (Asian clam), Sphaeroma quoyanum (a burrowing areas. It may thus be possible to use biotic homogeniza- isopod from Australia and New Zealand) and Spartina tion to monitor whether complementarity goals are alternifl ora (smooth cordgrass) have become among the being met. For example, if a network of reserves most important species in the bay in terms of both becomes more similar over time due to the loss of biomass and their role in controlling biological proc- unique species, this reduces complementarity (Rooney esses in the bay (Cohen & Carlton, 1998 ). et al. , 2007 ). Although the process of homogenization can create Importantly, any assessment of complementarity novel assemblages, global climate change is increas- related to conservation planning should be restricted ingly likely to magnify this effect. Thus, any prediction to indigenous species only. The inclusion of non- native of where novel assemblages will form needs to take into species could show increased biotic homogenization account not only non- native species introductions, but when, in reality, the full set of native species that the also global climate change and the individualistic reserve network was designed to conserve still occur. responses of species (native and non- native) to envi- This idea has much potential, but there are a few ronmental change (Chapters 4 , 7 ). Recent models caveats. For example, when dealing with a minimum suggest there will be substantial regions of the world set complementarity (each area contains distinctive with novel climates by 2100 (particularly in tropical species) goal, all areas may lose the same number of and sub- tropical regions) and also that some extant 242 Biological invasions and the homogenization of faunas and fl oras

create novel environmental conditions or, as Saxon et al . (2005) refers to them, ‘ environmental domains ’ . The disappearance or contraction of present environmental domains and the appearance of new domains will have profound consequences for most species and the identity of communities today. Climate change is expected to alter the effectiveness of environmental fi lters; to alter the likelihood of species establishing; to change pathways of species introductions; and to affect the impact of non- native species (Rahel & Olden, 2008 ). The combination of novel assemblages and altered biophysical conditions will result in new systems that have unknown functional characteristics, and whose processes and interactions are hard to predict (Hobbs et al. , 2006 ). Given the dynamic nature of species ’ distributions, current homogenization patterns and trends are likely Figure 9.7 A conceptual diagram showing how non- to change too. It is very diffi cult to predict the make - up analogue combinations of species arise in response to novel of novel assemblages, given that it is almost impossible climates. The set of climates in existence at two periods are to know which species will co - occur, whether they represented as open ellipses. Novel climates are the portions will interact and how altered climatic regimes will of the 21st century envelope that do not overlap 20th infl uence any interaction. Importantly, many of these century climates, and disappearing climates are the portions communities may be more, or less, similar across of the 20th century envelope that do not overlap 21st century climates. Species co- occur only if their fundamental locations than the native assemblages they replaced. niches simultaneously intersect with each other and the In other words, homogenization is not the only out- current climatic space. Future climate change may cause a come of the massive movement of species across the variety of ecological responses, including shifts in species’ globe. distributions (species 1– 3), community disaggregation Perhaps the only certainty is that conservation (species 1 and 3), new communities forming (species 2 and efforts will have to intensify to tackle the threat of 3), and extinction (species 4). From Figure 1 of Williams anthropogenically- assisted novel assemblages, and et al. (2007) ; copyright (2007) National Academy of society will be faced with some tough decisions as to Sciences, USA. what biodiversity it values.

FOR DISCUSSION climate types will have disappeared (Williams et al. , 1 How do natural patterns of species invasion differ 2007 ). from anthropogenically assisted species invasions, and Because climate is a primary control on species’ with what consequences? distributions and ecosystem processes, novel 21st 2 In the light of social demands and economic century climates may promote the formation of novel development, what are the most likely timescales and species associations and other ecological surprises. On scenarios of introduction, establishment and spread the other hand, the disappearance of some extant of non- native species in the future? climates increases the risk of extinction for species with 3 What are the ecological consequences of faunal and narrow geographical or climatic distributions, as well ﬂ oral homogenization? as the risk of disruption of existing communities 4 What are the temporal dynamics of taxonomic and (Figure 9.7 ). functional homogenization? Of greater concern, perhaps, is the combined effect 5 What are the primary environmental and biological of altered climate and other abiotic environmental drivers of biotic homogenization at different spatial characteristics (such as topography or soil type) which and temporal scales? Conservation planning in a changing world 243

6 How will rates and patterns of biotic homogeniza- of the new ecological world order. Global Ecology and tion respond to shifting pathways of species introduc- Biogeography , 15 , 1 – 7 . tions and future environmental change? McKinney , M.L. & Lockwood , J.L. ( 1999 ) Biotic homogeniza- 7 What novel species assemblages are likely to emerge tion: a few winners replacing many losers in the next mass in response to climate change? extinction . Trends in Ecology & Evolution , 14 , 450 – 453 . Olden , J.D. ( 2006 ) Biotic homogenization: a new research What might be the consequences of novel eco- 8 agenda for conservation biogeography . Journal of systems for biodiversity, ecosystem functioning, and Biogeography , 33 , 2027 – 2039 . human societies? Rahel , F.J. ( 2002 ) Homogenization of freshwater faunas . Annual Review of Ecology and Systematics , 33 , 291 – 315 . Riccardi , A. ( 2007 ) Are modern biological invasions an unprecedented form of global change? Conservation Biology , SUGGESTED READING 21 , 329 – 336 . Sax , D.F. , Stachowicz , J.J. , Brown , J.H. , Bruno , J.F. , Dawson , Elton , C.S. ( 1958 ) The ecology of invasions by animals and M.N. , Gaines , S.D. , Grosberg , R.K. , Hastings , A. , Holt , R.D. , plants . Methuen , London . Mayﬁ eld , M.M. , O ’ Connor , M.I. , & Rice , W.R. ( 2007 ) Hobbs , R.J. , Arico , S. , Aronson , J. , Baron , J.S. , Bridgewater , P. , Ecological and evolutionary insights from species inva- Cramer , V.A. , Epstein , P.R. , Ewel , J.J. , Klink , C.A. , Lugo , A.E. , sions . Trends in Ecology & Evolution , 22 , 465 – 471 . Norton , D. , Ojima , D. , Richardson , D.M. , Sanderson , E.W. , Strayer , D.L. , Eviner , V.T. , Jeschke , J.M. , & Pace , M.L. ( 2006 ) Valladares , F. , Vil à , M. , Zamora , R. , & Zobel , M. ( 2006 ) Understanding the long - term effects of species invasions . Novel ecosystems: theoretical and management aspects Trends in Ecology & Evolution , 21 , 645 – 651 .