Parasites as Drivers and Passengers of Human-Mediated Biological Invasions

There is evidence that host species that successfully establish alien populations, and that subsequently go on to spread across the new environment, tend to have escaped from parasites that afflict them in their native range (Mitchell and Power 2003; Torchin et al. 2003; Lymbery et al. 2010; Roche et al. 2010; Prior and Hellmann 2015). For example, Torchin et al. (2003) showed that parasite species richness and prevalence was generally lower in the alien than the native range for a variety of alien species, including molluscs, crustaceans, fishes, amphibians, reptiles, mammals and birds. Mitchell and Power (2003) showed that plant species introduced to the USA were infected by, on average, 84% fewer fungi and 24% fewer virus species in their alien versus their native ranges. Successful alien species may also tend to harbour fewer parasites than native species in the same community (Roche et al. 2010). For example, in Northern Ireland, the invading alien amphipod Gammarus pulex has lower parasite diversity than the native G. duebeni celticus, and also lower prevalence and burden of the two parasite species that the alien and native amphipods share (Dunn 2009). These patterns are concordant with release from parasites as a determinant of success in alien invasions.

However, there is as yet little convincing evidence that release from parasites is actually a determinant of success in alien host population establishment or spread. There are at least two reasons for this. First, it is difficult to demonstrate for any given alien host population that its success was due to enemy release and not to other factors. It is necessary to show that the native host population is controlled by enemies, that the alien host population has escaped this control, and that this escape is the key determinant of success (Prior et al. 2015). There are examples where release from enemies has occurred but does not appear to underlie success (e.g. McDonald and Kotanen 2010; Prior et al. 2014). Second, the mechanisms that lead to escape from parasites should apply to all alien host populations—successful or not (see below). Under the ERH, it is necessary for alien host populations that successfully establish to have benefitted more from parasite release than those that fail to establish, and likewise for those species that have versus have not spread (Blackburn et al. 2015a). Studies are only informative on these questions if they have compared the extent of escape from parasitism in host populations that are introduced and become established versus those that are introduced but do not, or in host populations that establish and spread to varying extents (van Kleunen et al. 2010). We are aware of only two studies that have adopted this approach. Mitchell and Power (2003) showed that, amongst plant species listed as natural area invaders, species that experienced more complete pathogen release were more widely invasive. However, their measure of invasion is not a direct measure of extent of spread, and their analysis is not robust to the exclusion of a single outlier. Van Kleunen and Fischer (2009) showed that the geographic spread of alien plants introduced from North America to Europe was negatively associated with their release from fungal pathogens, contrary to the ERH. Neither of these studies explores the extent to which the species were under enemy regulation in their native ranges.

There is abundant evidence that natural enemies regulate natural populations of animals and plants (Sih et al. 1985; Prior et al. 2015), and successes in the biocontrol of aliens demonstrate that reacquainting hosts with their parasites can have dramatic impacts on populations of the former (Lafferty et al. 2005). Hence, it might be considered surprising that there is so little direct support for an effect of escape from parasites on alien host invasion success. The reason is undoubtedly due in part to the absence of information with which to test the influence of parasites on establishment success: there are simply no data on the parasite loads of failed introductions with which to compare successes (van Kleunen et al. 2010). However, even if there were, we might be unlikely to identify an effect. Translocated host populations may lose parasites for three reasons. First, introduced populations tend to consist of relatively small numbers of translocated individuals (Blackburn et al. 2009). These individuals may by chance lack parasites due to sampling effects (Paterson et al. 1999; Prenter et al. 2004; MacLeod et al. 2010). Second, parasites may be lost as a result of reduced opportunities for transmission in the alien environment, for example, because host populations are typically small and host densities low in the early stages of an invasion (Dunn 2009). Third, translocated individuals with parasites (or the parasites themselves) may consistently die in transit (Prenter et al. 2004). This may especially be the case for highly virulent parasites (Strauss et al. 2012). Parasites lost in this way may be unable to reach new environments (Prenter et al. 2004), perhaps unless transit times are greatly reduced. This third reason would apply to all translocated hosts, meaning that successful and failed introductions could not be distinguished on the basis of parasite loss in this way.

The first two of the reasons why alien hosts might lose parasites would be expected to lead to higher likelihoods of loss, and hence higher establishment success under the ERH, when fewer individuals were translocated (Drake 2003). However, there is in fact a robust and consistent positive relationship between establishment success (and indeed extent of spread) and the number of individuals introduced (“propagule pressure”) for alien populations (Lockwood et al. 2005; Colautti et al. 2006; Hayes and Barry 2008; Simberloff 2009; Blackburn et al. 2015a, b). This latter relationship probably arises because larger propagule pressure buffers against the stochastic processes (demographic, environmental, genetic or Allee) to which small, introduced populations will be vulnerable (Duncan et al. 2014; Blackburn et al. 2015b). These effects seem to outweigh any benefits that smaller introduced populations may accrue by escaping parasites (Drake 2003; Dunn 2009). Drake (2003) suggests that enemy release may mediate variation in the subsequent extent of spread, but there is currently no good evidence that it does. It is also hard to see how it would, given that propagule pressure is also positively related to spread (Blackburn et al. 2015b).

Positive relationships between success and propagule pressure suggest that escape from parasites is unlikely to be a primary driver of host invasion success, but it could still mediate variation around the propagule pressure relationship. Species vary in the extent to which their native populations are regulated by natural enemies, and so enemy release may matter more for the success of host species for which enemy impacts are naturally greater (Prior et al. 2015). For a given propagule pressure, host success may therefore be higher for species with more to gain by escaping their enemies (Figure 1).

Escape from parasites seems unlikely to distinguish successful from unsuccessful invasions, but an alternative idea is that success is greater for host species that bring their parasites with them. Theory predicts that the virulence of parasites will be low in hosts that have evolved with the parasite, but high in new hosts because of lack of evolved immunological resistance (Schmid-Hempel 2011). The parasites arriving in alien hosts are also expected to be relatively benign to those hosts, because otherwise the hosts are likely to have died in transit (Strauss et al. 2012). Not all parasites are equally likely to make the jump into new hosts, with generalist and vector-borne parasites being the most likely (Prenter et al. 2004; Hatcher et al. 2012). Nevertheless, if alien parasites can infect native species in the recipient environment (i.e. if there is parasite ‘spillover’; Daszak et al. 2000), if they are indeed more virulent in these naïve hosts, and if their negative impacts on the native species increase the likelihood that the alien host establishes and spreads, then these parasites may be considered to be novel weapons in the struggle between alien and native hosts. The NWH could also operate via ‘spillback’ (Daszak et al. 2000; Kelly et al. 2009). Kelly et al. (2009) argue that in some cases a native parasite may actually be less virulent in an alien host and facilitate invasion through spillback from alien to native host (see also Strauss et al. 2012).

There are a number of high-profile examples of host invasions that are likely to have been facilitated by parasite spillover to native competitors, usually close phylogenetic relatives of the alien species (Strauss et al. 2012). The classic example is the replacement of the red squirrel (Sciurus vulgaris) by the grey (S. carolinensis) in the UK, which has been mediated at least in part by parapoxvirus introduced from North America along with the grey squirrels (Sainsbury and Gurnell 1995; Tompkins et al. 2003; Bosch and Lurz 2012). The virus is highly virulent in red but not grey squirrels, and the greys act as a reservoir for it. While the grey squirrel is also a superior competitor, features of the invasion, such as the disappearance of red squirrels from areas before grey squirrels arrive, suggest that the virus is facilitating the invasion. Other examples of parasite-mediated invasions include the red signal crayfish (Pacifastacus leniusculus) in the UK and the harlequin ladybird (Harmonia axyridis) in Europe and North America (Strauss et al. 2012; Vilcinskas 2015). Parasites have also been implicated in plant invasions, although here the mechanism is spillback; spillover may be less common in plants because most parasites cannot accompany those species introduced as seeds (Mitchell and Power 2003; Strauss et al. 2012).

As with the ERH (albeit in reverse), it is not enough to show that alien hosts are accompanied by parasites to provide a valid test of the NWH: rather, variation in success must be linked to variation in parasite impacts. As with the ERH, there are simply no data on the parasites of species that failed to establish to compare against those that succeeded, and therefore, the validity of the NWH for the establishment stage of invasion is currently untestable. However, in this case, the robust positive relationship between establishment success (and extent of spread) and numbers of individuals introduced is at least consistent with the idea that success is higher for species that are more likely to bring parasites with them. There is more promise in testing the NWH for variation in the extent of alien spread, and the negative relationship between the geographic range size of alien plants and their release from fungal pathogen load found by van Kleunen and Fischer (2009) is also consistent with the hypothesis. Further tests in this vein would be a useful start in evaluating the potential generality of the NWH, on the assumption that alien species harbouring more alien parasites are more likely to be wielding a novel weapon.

Stronger evidence for the importance of novel weapons would come from demonstrations that more successful alien hosts are more likely to have reduced populations of their native natural enemies through parasite spillover (or spillback). However, any such test would need to overcome considerable hurdles. The effects of parasites can be difficult to detect, even in well-studied invasions. For example, there was a gap of more than 60 years between the first identification of the squirrel pox disease and the first suggestion that it might have a role in the decline of the red squirrel in the UK (Strauss et al. 2012). Parapoxvirus kills red squirrels very quickly, and so is rarely seen in the wild. Inconspicuousness is likely to be a feature of the kinds of highly virulent parasites that are most likely to regulate host populations (Anderson and May 1981). Furthermore, while there have undoubtedly been obvious and catastrophic population declines as a result of alien parasites (e.g. chestnut blight in North America, rinderpest in Africa, the chytrid fungus worldwide), most effects are likely to relate to less virulent but nonetheless persistent and important sub-lethal infections (Prenter et al. 2004). Effects of such parasites will be even harder to demonstrate. Finally, it is not enough to show that native and alien host species share parasites—one must demonstrate that the parasite has deleterious impacts on the native species, and improves the performance of the alien as a result (Strauss et al. 2012). Perhaps the best we can hope for is evidence that novel weapons matter for some invasions, but not how often they matter.

The theoretical expectation that parasite virulence will be lower for co-evolved than for novel, naïve hosts (Schmid-Hempel 2011) may explain why novel weapons work, but should apply equally to alien host species encountering novel parasites endemic to the new environment. Indeed, arguably novel weapons should work more strongly against aliens. Alien species tend to be introduced in low numbers and therefore likely missing many of their natural parasites. Alien species are introduced into environments relatively species rich and these communities will tend to have relatively greater parasite species richness (Krasnov et al. 2004; Thieltges et al. 2011). In general, therefore, and acknowledging well-known counter-examples (e.g. avian malaria on Hawaii; Warner 1968), one would expect alien species to encounter more novel parasites than they bring. If novel weapons matter, we would expect alien host species to establish and spread less well in native assemblages with higher parasite diversity, as predicted by the BRH.

Biotic resistance can of course derive from elements of the native biota other than parasites, such as predators or competitors. Most tests of the BRH have addressed general relationships between establishment success or extent of alien host spread and indirect correlates of community richness, such as latitude or island versus continental location, or direct measures of community richness other than that of parasites (Blackburn et al. 2011b). These tests are far from convincing in their support for the BRH (Sol 2000; Blackburn et al. 2011b). As far as we are aware, there are as yet no studies that have explicitly tested whether native parasites are responsible for biotic resistance to aliens, although such negative relationships between correlates of native richness and alien success as do exist may be down to parasites. Once again, we would note the difficulty of demonstrating direct effects of parasites on the failure of alien host populations to establish, as failures typically disappear without study; the effects of biotic resistance may be greatly underestimated. Comparative analyses of relative levels of alien host success (establishment or spread) in areas with different parasite assemblages would be possible, though.

There are also few clear examples where the spread of alien host species into new areas have been prevented by native parasites. One classic example from agriculture relates to the impact of the protozoan parasite Trypanosoma brucei on cattle, which has acted as a major constraint to livestock production in parts of Africa (Perkins et al. 2008). The recruitment of native diseases may be responsible for at least some of the sudden and unexplained population crashes observed in some alien populations (Simberloff and Gibbons 2004); the rate of enemy accumulation seems to be driven by the extent of the alien host distribution rather than residence time (Strong et al. 1977; Branco et al. 2015). However, as noted above, the effects of parasites can be difficult to detect even in well-studied populations, and attributing an alien host population crash to native parasites would require extreme serendipity in terms of the type and timing of research on the alien.

One argument against a general effect of biotic resistance by parasites comes from tests of Darwin’s observation that it should be easier for alien host species with no close phylogenetic relatives to invade new areas, because they will tend to share fewer natural enemies with the native species (Darwin 1859). This idea has become known as Darwin’s Naturalisation Hypothesis, although Darwin did also recognise that the reverse could be true if shared environmental preferences mattered more than shared natural enemies (Diez et al. 2008). However, tests of the hypothesis have been equivocal in their support for it (Thuiller et al. 2010). If biotic resistance (of any kind) does affect the success of alien species, its signature has not yet been detected in patterns of relatedness between aliens and natives.

Invasions begin with individuals being transported to locations outside their natural geographic range, and introduced to the new environment there (Blackburn et al. 2011a)—we term these combined stages “translocation”. The transport and introduction stages are often considered together, as here, because we rarely have data on species that have been transported but not introduced: the first evidence that transport has occurred is usually when we observe alien host species already in the wild, especially for host species translocated by accident. Translocated host species tend either to be actively selected by humans (and therefore probably considered beneficial in some way) or, if translocated accidentally, then host species more likely to be chosen at random. The likelihood of translocation is driven by the availability of individuals in the native range (Hulme 2009; Blackburn et al. 2015b). Thus, more widespread and abundant host species are more likely to be translocated, and this is true on average regardless of whether host species are translocated deliberately or accidentally (Blackburn and Duncan 2001; Hulme 2009).

These same criteria will apply to parasite species, just as to their hosts, albeit with the additional complication that most parasites translocated accidentally depend on the translocation of their hosts (Lymbery et al. 2014). Thus, parasite species may be translocated deliberately because they are themselves desirable species, for example, biocontrol agents against (possibly alien) pests (Beirne 1975; Hopper and Roush 1993). Alien parasites should be more likely to be translocated accidentally if they are parasites of desirable (to humans) hosts, or of hosts more likely to be translocated accidentally, or if they have free-living stages that are likely to be translocated accidentally. However, even parasites that do inhabit host species may still fail to be translocated if they are not present in the specific host individuals translocated—termed ‘missing the boat’ (Paterson and Gray 1997). The likelihood that this happens should depend on the prevalence and generalism of the parasite, as parasites with higher prevalence in translocated hosts, or that infect a wide range of hosts, are more likely by chance to make it onto the boat (MacLeod et al. 2010).

What evidence there is for parasites is consistent with the idea that availability does indeed influence the likelihood of translocation. Thus, Ewen et al. (2012) found that alien strains of avian malaria in New Zealand had larger native geographic ranges, and were also found in a broader taxonomic range of native host bird species. Although Ewen et al. (2012) had no data on which strains where actually translocated (those present now may only be a small fraction of these), the patterns are consistent with a positive effect of availability (see also next section).

Parasites that make it on to the ‘boat’ may still fail to arrive at the boat’s destination if their hosts die en route—and as discussed above, the presence of the parasite may increase the likelihood of that happening. We would therefore expect a negative relationship between the probability of successful translocation and parasite virulence, given that hosts of more virulent parasites are less likely to survive the voyage (Strauss et al. 2012; Lymbery et al. 2014). At present, we are unaware of any evidence on the impact of virulence on the likelihood that parasites fail in transit. Nevertheless, there is evidence that hosts do frequently die in transit (e.g. Pipek et al. 2015), and the impact of parasites is one possible cause.

Following translocation, a species must establish a viable population if it is to maintain itself as an alien at the new location (Blackburn et al. 2011a). New environments pose potentially significant challenges to alien population establishment, and only a fraction of translocated species succeed (the much-discussed “Tens Rule” suggests a typical range of 5–20%; see Jeschke 2014). These challenges will be compounded for alien parasites because they are dependent first on the establishment success of their hosts. Parasites that catch the boat and survive the voyage will not become aliens if their hosts fail to establish following arrival; this is termed ‘sinking with the boat’ (MacLeod et al. 2010). The presence of the parasite may once again affect the likelihood of that happening, although this time the effect may be positive or negative (Figure 2).

The most robust and consistent determinant of the success of alien host species is propagule pressure (see above). A larger host population size is also likely to increase a parasite’s establishment success, by increasing the likelihoods that the parasite has been transported, that some infected hosts have survived the journey, and that new hosts are available to ensure transmission in the new environment (MacLeod et al. 2010).

MacLeod et al. (2010) assessed the importance of different processes in determining whether chewing lice successfully established along with their hosts: bird species introduced from Europe to New Zealand. They found that approximately two-thirds of the species of feather lice present on bird species in their native ranges were absent from these hosts in New Zealand. MacLeod et al. (2010) then used simulations to assess the likelihood that louse species would have been lost at different invasion stages, on the basis of data on the composition and prevalence of louse assemblages in the native and alien ranges, and on the numbers of individuals of different bird species introduced. Their analysis showed that few louse species (in the range of 8–20% of those lost) were likely to have missed the boat, because sufficiently high numbers of birds were introduced that most lice species would have been translocated too. Rather, most louse species lost (around half) were most likely to be absent because their hosts failed to establish (they ‘sank with the boat’). Host bird populations were more likely to fail to establish in New Zealand if they comprised lower numbers of individuals (Veltman et al. 1996; Duncan 1997; Green 1997; Cassey 2001; Duncan et al. 2006). Clearly, the situation is likely to vary on a case-by-case basis, depending on the numbers of hosts transported and the prevalence (and any harmful effects) of parasites. It is also likely to depend on the parasites’ host ranges, as more generalist parasites presumably are more likely to be present on at least one host that establishes.

The second most common cause of failure in the louse species studied by MacLeod et al. (2010) was what they termed being ‘lost overboard’: these are parasites that failed to establish alien populations despite being unlikely to have missed the boat, and despite having hosts that successfully established. These species may have died in transit (dealt with above), or failed to establish after translocation. If the latter, then failure may again have been because numbers were against them. As with their hosts, parasites may fail to establish for stochastic reasons if introduced in low numbers (e.g. <5 infected hosts), even in otherwise suitable circumstances (Hatcher et al. 2012). Parasites with single hosts and density-dependent transmission also have a threshold host density below which persistence is unlikely, equivalent to an Allee effect in host populations (Hatcher et al. 2012). Other specific features of the introduction event may also affect success. For example, seasonality (e.g. introduction date) can affect the transmission of parasites by determining the presence of insect vectors (Hatcher et al. 2012).

As well as factors specific to a given introduction event, such as numbers introduced or date, alien species establishment success is influenced by characteristics of the introduction location and of the species introduced (Duncan et al. 2003). The kinds of location-level and species-level effects that influence parasite establishment success are likely to be somewhat different to those for their hosts. The environment for the parasite is the host, and so as long as the parasite’s host establishes, a suitable environment is at least partly guaranteed. Nevertheless, other location-level features can still influence success. Most notably, parasites that are vector-borne or have complex life cycles require the presence of suitable vectors or intermediate hosts, and will not be able to establish in environments lacking them (Prenter et al. 2004; Lymbery et al. 2014). Thus, it was only after the introduction of the alien mosquito Culex quinquefasciatus to Hawaii in 1826 that avian malaria could establish in the resident avifauna of the islands (Warner 1968).

A corollary of the requirement for vectors or intermediate hosts is that directly or vertically transmitted parasites are more likely to find the novel environment suitable, assuming that their hosts do (Hatcher and Dunn 2011). Lymbery et al. (2014) found that 64% of co-introduced alien parasites in their literature survey had direct life cycles, but noted that this could be affected by a taxonomic bias in their data towards monogeneans, all of which have direct life cycles. Direct and indirect life cycles were more or less equally represented if monogeneans were excluded. Parasites may also be more likely to establish if they have a broad host range, assuming that this translates into a higher availability of suitable hosts in the new location. Thus, alien strains of avian malaria successfully established in New Zealand have a broader taxonomic range of native host bird species than expected by chance (Ewen et al. 2012). Host range may also interact with life cycle, as vector-borne parasites are more likely to jump hosts (Hatcher et al. 2012). This spillover will be more likely when contact with a novel host is more frequent (Hatcher et al. 2012).

Nevertheless, the presence of novel hosts may actually hamper the establishment of a parasite if the parasite has lower fitness in the new host, as may well be the case when the host and parasite have not co-evolved (Dunn 2009). Most studies of host-parasite interactions consider fitness consequences for the host, but it is the fitness of the parasite that is relevant in the context of parasite invasions. Parasites can establish when their basic reproductive number R ₀  > 1: that is, when each primary case of infection results in more than one secondary case (Anderson and May 1982). Transmission into novel hosts in which the parasite cannot complete its life cycle, or for which its virulence is so high that the host dies before it can pass on the infection, can both lower R ₀ and cause establishment failure in the parasite (Hatcher et al. 2012). Models of alien bird species establishment also suggest that a high R ₀ (for birds, the average number of daughters produced per female over her lifetime) is a key determinant of success (Cassey et al. 2014), implying that demography is likely to matter for both parasites and their hosts (Sol et al. 2012).

Invasive spread by an alien species can be viewed as a continuation of the establishment phase, in which the processes determining establishment are simply played out across a wider environmental arena (Blackburn et al. 2015b). Nevertheless, spread may be facilitated by evolutionary changes in the parasite or host populations following establishment (Hatcher et al. 2012). For example, the evolution of reduced virulence in a novel host in the alien environment may elevate R ₀ > 1 for the parasite, and hence promote its spread through the novel host population. Conversely, evolutionary changes that allow host jumps may cause the parasite to act as a novel weapon, promoting its spread via an expansion of its original (alien) host (see above). Selection is most likely to drive evolutionary changes in situations where R ₀ is close to (but below) 1 (Holt et al. 2005), as populations with R ₀ ≪ 1 will die out too rapidly for selection to influence their trajectory, while populations with R ₀ > 1 will grow without the need for evolutionary adaptations.