Invader immunology: invasion history alters immune system function in cane toads (Rhinella marina) in tropical Australia

Because an individual's investment into the immune system may modify its dispersal rate, immune function may evolve rapidly in an invader. We collected cane toads (Rhinella marina) from sites spanning their 75‐year invasion history in Australia, bred them, and raised their progeny in standard conditions. Evolved shifts in immune function should manifest as differences in immune responses among the progeny of parents collected in different locations. Parental location did not affect the offspring's cell‐mediated immune response or stress response, but blood from the offspring of invasion‐front toads had more neutrophils, and was more effective at phagocytosis and killing bacteria. These latter measures of immune function are negatively correlated with rate of dispersal in free‐ranging toads. Our results suggest that the invasion of tropical Australia by cane toads has resulted in rapid genetically based compensatory shifts in the aspects of immune responses that are most compromised by the rigours of long‐distance dispersal.     

Stress and immunity at the invasion front: a comparison across cane toad (Rhinella marina) populations

At an invasion front, energetic and physiological trade‐offs may differ from those at the range‐core as a result of selection for enhanced dispersal, combined with a low density of conspecifics (which reduces pathogen transmission and competition for food). We measured traits related to energy stores and immunity in wild cane toads (Rhinella marina) across a 750‐km transect from their invasion front in tropical Australia, back into sites colonized 21 years earlier. Several traits were found to vary with population age; some linearly and others in a curvilinear manner. The relative size of spleens and fat bodies was highest in the oldest and newest populations, where rates of lungworm infection were lowest. Toads from older populations produced more corticosterone in response to a standardized stressor, and had higher lymphocyte counts (but lower basophil counts). The amount of skin swelling elicited by phytohaemagglutinin injection did not vary geographically, although recruitment of leukocytes to the injected tissue was higher in toads from long‐colonized areas. Because this was a field‐based study, we cannot differentiate the effects of population age, toad density or pathogen pressure on our measures of stress and immune responses, nor can we distinguish whether the causation involves hard‐wired adaptive processes or phenotypically plastic responses. Nonetheless, our data demonstrate substantial variation in immune systems among toads at varying distances from an invasion front, showing that a biological invasion imposes strong pressures on physiological systems of the invader.     

Locomotor performance in an invasive species: cane toads from the invasion front have greater endurance, but not speed, compared to conspecifics from a long-colonised area

Cane toads (Bufo marinus) are now moving about 5 times faster through tropical Australia than they did a half-century ago, during the early phases of toad invasion. Radio-tracking has revealed higher daily rates of displacement by toads at the invasion front compared to those from long-colonised areas: toads from frontal populations follow straighter paths, move more often, and move further per displacement than do toads from older (long-established) populations. Are these higher movement rates of invasion-front toads associated with modified locomotor performance (e.g. speed, endurance)? In an outdoor raceway, toads collected from the invasion front had similar speeds, but threefold greater endurance, compared to conspecifics collected from a long-established population. Thus, increased daily displacement in invasion-front toads does not appear to be driven by changes in locomotor speed. Instead, increased dispersal is associated with higher endurance, suggesting that invasion-front toads tend to spend more time moving than do their less dispersive conspecifics. Whether this increased endurance is a cause or consequence of behavioural shifts associated with rapid dispersal is unclear. Nonetheless, shifts in endurance between frontal and core populations of this invasive species point to the complex panoply of traits affected by selection for increased dispersal ability on expanding population fronts.     

Reid's paradox revisited: the evolution of dispersal kernels during range expansion

Current approaches to modeling range advance assume that the distribution describing dispersal distances in the population (the "dispersal kernel") is a static entity. We argue here that dispersal kernels are in fact highly dynamic during periods of range advance because density effects and spatial assortment by dispersal ability ("spatial selection") drive the evolution of increased dispersal on the expanding front. Using a spatially explicit individual-based model, we demonstrate this effect under a wide variety of population growth rates and dispersal costs. We then test the possibility of an evolved shift in dispersal kernels by measuring dispersal rates in individual cane toads (Bufo marinus) from invasive populations in Australia (historically, toads advanced their range at 10 km/year, but now they achieve >55 km/year in the northern part of their range). Under a common-garden design, we found a steady increase in dispersal tendency with distance from the invasion origin. Dispersal kernels on the invading front were less kurtotic and less skewed than those from origin populations. Thus, toads have increased their rate of range expansion partly through increased dispersal on the expanding front. For accurate long-range forecasts of range advance, we need to take into account the potential for dispersal kernels to be evolutionarily dynamic.     

The evolution of growth rates on an expanding range edge

Individuals in the vanguard of a species invasion face altered selective conditions when compared with conspecifics behind the invasion front. Assortment by dispersal ability on the expanding front, for example, drives the evolution of increased dispersal, which, in turn, leads to accelerated rates of invasion. Here I propose an additional evolutionary mechanism to explain accelerating invasions: shifts in population growth rate (r). Because individuals in the vanguard face lower population density than those in established populations, they should (relative to individuals in established populations) experience greater r-selection. To test this possibility, I used the ongoing invasion of cane toads (Bufo marinus) across northern Australia. Life-history theory shows that the most efficient way to increase the rate of population growth is to reproduce earlier. Thus, I predict that toads on the invasion front will exhibit faster individual growth rates (and thus will reach breeding size earlier) than those from older populations. Using a common garden design, I show that this is indeed the case: both tadpoles and juvenile toads from frontal populations grow around 30 per cent faster than those from older, long established populations. These results support theoretical predictions that r increases during range advance and highlight the importance of understanding the evolution of life history during range advance.     

Investment in seed dispersal structures is linked to invasiveness in exotic plant species of south-eastern Australia

Naturalized plant species disperse their populations over considerable distances to become invasive. We tested the hypothesis that this shift from naturalization to invasion is facilitated by increased investment of resources in seed dispersal appendages, using an assemblage of naturalized plants of south-eastern Australia. Compared with non-invasive species, we found in both cross-species and independent-contrasts analyses that invasive species invested more heavily in seed dispersal appendages, regardless of the structure present on the seed associated with the mode of dispersal (e.g., wings versus fleshy fruits). Invasive species such as Lonicera japonica, Hedera Helix and Acetosa sagittata were found to invest as much as 60–70% of total diaspore mass in dispersal appendages. The positive relationship between dispersal investment and invasion success was still prevalent after controlling for the effects of plant growth form, seed mass and capacity for vegetative growth. Our findings demonstrate that a plant’s investment in dispersal appendages helps to overcome the dispersal barrier in the shift from naturalization to invasion.     

Toad’s tongue for breakfast: exploitation of a novel prey type,the invasive cane toad,by scavenging raptors in tropical Australia

Although interest in the ecological impacts of invasive species has largely focused on negative effects, some native taxa may benefit from invader arrival. In tropical Australia, invasive cane toads (Bufo marinus) have fatally poisoned many native predators (e.g., marsupials, crocodiles, lizards) that attempt to ingest the toxic anurans, but birds appear to be more resistant to toad toxins. We quantified offtake of dead (road-killed) cane toads by raptors (black kites (Milvus migrans) and whistling kites (Haliastur sphenurus)) at a site near Darwin, in the Australian wet-dry tropics. Raptors readily took dead toads, especially small ones, although native frogs were preferred to toads if available. More carcasses were removed in the dry season than the wet season, perhaps reflecting seasonal availability of alternative prey. Raptors appeared to recognize and avoid bufotoxins, and typically removed and consumed only the toads’ tongues (thereby minimizing toxin uptake). The invasion of cane toads thus constitutes a novel prey type for scavenging raptors, rather than (as is the case for many other native predators) a threat to population viability.     

The Archipelago of Fernando de Noronha: An Intriguing Malformed Toad Hotspot in South America

Malformed anurans raise concern among scientists, because deformities may relate to the recent global crisis among amphibian populations, although declining populations also may be associated with other causes (e.g., diseases, over-exploitation, and land use/land cover change). We examined a sample of toads (Rhinella jimi, Bufonidae) from an introduced population in the Archipelago of Fernando de Noronha, Brazil where malformations of anurans were thought to be high. Our sample of 159 specimens from the site revealed that 44.6% of all specimens had one or more malformations. Incidence of malformed toads on the mainland sites was substantially lower: 10.5% at Itamaracá, and 3.7% at Propriá. We describe the malformations observed, including six undescribed types of malformation of anurans, and we pose possible hypotheses to explain this high incidence of malformed toads. In addition to existing hypotheses, we suggest for the first time the hypothesis that lack of predation pressures contributes to numbers of malformed toads. We indicate the need of specific studies to understand the causes of malformations in the R. jimi population of Fernando de Noronha, which is thought to be extreme foci of malformed amphibians in the world. Our results may improve local conservation action plans as this is an alien population that may be affecting endemic fauna, and may affect populations in other parts of the world, because toad species of the genus Rhinella are recognized as exceptional colonizers. More importantly, unknown variables in these toads’ environment are evidently affecting toads during development, which should be a concern for all species that inhabit the area, perhaps even humans.     

Evolutionarily accelerated invasions: the rate of dispersal evolves upwards during the range advance of cane toads

Human activities are changing habitats and climates and causing species' ranges to shift. Range expansion brings into play a set of powerful evolutionary forces at the expanding range edge that act to increase dispersal rates. One likely consequence of these forces is accelerating rates of range advance because of evolved increases in dispersal on the range edge. In northern Australia, cane toads have increased their rate of spread fivefold in the last 70 years. Our breeding trials with toads from populations spanning the species' invasion history in Australia suggest a genetic basis to dispersal rates and interpopulation genetic variation in such rates. Toads whose parents were from the expanding range front dispersed faster than toads whose parents were from the core of the range. This difference reflects patterns found in their field-collected mothers and fathers and points to heritable variance in the traits that have accelerated the toads' rate of invasion across tropical Australia over recent decades. Taken together with demonstrated spatial assortment by dispersal ability occurring on the expanding front, these results point firmly to ongoing evolution as a driving force in the accelerated expansion of toads across northern Australia.     

May the (selective) force be with you: Spatial sorting and natural selection exert opposing forces on limb length in an invasive amphibian

Spatial sorting on invasion fronts drives the evolution of dispersive phenotypes, and in doing so can push phenotypes in the opposite direction to natural selection. The invasion of cane toads (Rhinella marina) through tropical Australia has accelerated over recent decades because of the accumulation of dispersal‐enhancing traits at the invasion front, driven by spatial sorting. One such trait is the length of the forelimbs: invasion‐front toads have longer arms (relative to body length) in comparison with populations 10–20 years after invasion. Such a shift likely has fitness consequences: an increase of forearm length would decrease the strength with which a male could cling to a female during amplexus and so render such a male less competitive in competition for mates, compared to short‐armed conspecifics. Our laboratory trials of attachment strength confirmed that males with relatively longer arms were easier to displace, and competition trials show higher duration of amplexus for males with shorter arms. Together with the sharp cline in limb length observed behind the invasion front, these results imply an opposition of selective forces: spatial sorting optimizes dispersal, but as this force wanes behind the invasion front, we see the primacy of natural selection reassert itself.     

Virgins in the vanguard: low reproductive frequency in invasion‐front cane toads

The rapid evolution of increased dispersal rate during a population's range expansion provides a unique opportunity to detect trade‐offs between dispersal and reproduction. If a high reproductive rate slows down an individual's dispersal, vanguard individuals should exhibit a lower reproductive output than conspecifics from long‐colonized areas. In the present study, we demonstrate a reduction in reproductive rate in highly dispersive invasion‐front populations of cane toads in tropical Australia.     

Higher investment in flight morphology does not trade off with fecundity estimates in a poleward range‐expanding damselfly

1. Evolutionary increases in dispersal‐related traits are frequently documented during range expansions. Investment in flight‐related traits is energetically costly and a trade‐off with fecundity may be expected during range expansion. 2. However, in contrast to wing‐dimorphic species, this trade‐off is not general in wing‐monomorphic species. In the absence of a dispersal‐‐fecundity trade‐off, an increased investment in clutch size at the expansion front is expected possibly at a cost of reduced offspring size. 3. The study evaluated investment in female flight morphology and fecundity‐related traits (clutch size, hatchling size) and potential trade‐offs among these traits in replicated populations of the poleward range‐expanding damselfly Coenagrion scitulum. 4. Females at the expansion front had a higher relative thorax length, indicating an increased investment in flight; this can be explained by spatial sorting of dispersal ability or in situ natural selection at the expansion front. Edge females produced larger hatchlings, however, this pattern was totally driven by the population‐specific thermal larval regimes and could not be attributed to the range expansion per se. By contrast, clutch sizes did not differ between core and edge populations. There was no signal of a dispersal–fecundity trade‐off either for a trade‐off between clutch size and hatchling size. 5. These results indicate that evolution of a higher dispersal ability at the expansion front of C. scitulum does not trade off with investment in fecundity, hence a dispersal–fecundity trade‐off is unlikely to slow down range expansion of this species.     

Shifting dispersal modes at an expanding species’ range margin

While it is generally recognized that noncontiguous (long‐distance) dispersal of small numbers of individuals is important for range expansion over large geographic areas, it is often assumed that colonization on more local scales proceeds by population expansion and diffusion dispersal (larger numbers of individuals colonizing adjacent sites). There are few empirical studies of dispersal modes at the front of expanding ranges, and very little information is available on dispersal dynamics at smaller geographic scales where we expect contiguous (diffusion) dispersal to be prevalent. We used highly polymorphic genetic markers to characterize dispersal modes at a local geographic scale for populations at the edge of the range of a newly invasive grass species (Brachypodium sylvaticum) that is undergoing rapid range expansion in the Pacific Northwest of North America. Comparisons of Bayesian clustering of populations, patterns of genetic diversity, and gametic disequilibrium indicate that new populations are colonized ahead of the invasion front by noncontiguous dispersal from source populations, with admixture occurring as populations age. This pattern of noncontiguous colonization was maintained even at a local scale. Absence of evidence for dispersal among adjacent pioneer sites at the edge of the expanding range of this species suggests that pioneer populations undergo an establishment phase during which they do not contribute emigrants for colonization of neighbouring sites. Our data indicate that dispersal modes change as the invasion matures: initial colonization processes appear to be dominated by noncontiguous dispersal from only a few sources, while contiguous dispersal may play a greater role once populations become established.     

The accelerating invasion: dispersal rates of cane toads at an invasion front compared to an already-colonized location

Evolutionary theory predicts that individuals at an expanding range edge will disperse faster than conspecifics in long-colonized locations, but direct evidence is rare. Previous reports of high rates of dispersal of cane toads (Rhinella marina) at the invasion front have been based on studies at a single site in the Northern Territory. To replicate the earlier work, we radio-tracked free-ranging toads in the Kimberley region of northwestern Australia (at the westward-spreading invasion front) and 500 km northeast, on the Adelaide River floodplain of the Northern Territory (where toads had already been present for 6 years). For comparison, we also radio-tracked native frogs (Litoria caerulea and L. splendida) at the same sites. Consistent with the earlier reports, invasion-front cane toads travelled further per day, were more highly directional, and re-used refuge sites less frequently, than did conspecifics from an already-colonized site. In contrast, native frogs showed similar movement patterns in the two study areas. Our results confirm previous reports, and suggest that accelerated dispersal may be a common feature of individuals at the vanguard of a biological invasion.     

Differences in developmental strategies between long‐settled and invasion‐front populations of the cane toad in Australia

Phenotypic plasticity can enhance a species’ ability to persist in a new and stressful environment, so that reaction norms are expected to evolve as organisms encounter novel environments. Biological invasions provide a robust system to investigate such changes. We measured the rates of early growth and development in tadpoles of invasive cane toads (Rhinella marina) in Australia, from a range of locations and at different larval densities. Populations in long‐colonized areas have had the opportunity to adapt to local conditions, whereas at the expanding range edge, the invader is likely to encounter challenges that are both novel and unpredictable. We thus expected invasion‐vanguard populations to exhibit less phenotypic plasticity than range‐core populations. Compared to clutches from long‐colonized areas, clutches from the invasion front were indeed less plastic (i.e. rates of larval growth and development were less sensitive to density). In contrast, those rates were highly variable in clutches from the invasion front, even among siblings from the same clutch under standard conditions. Clutches with highly variable rates of growth and development under constant conditions had lower phenotypic plasticity, suggesting a trade‐off between these two strategies. Although these results reveal a strong pattern, further investigation is needed to determine whether these different developmental strategies are adaptive (i.e. adaptive phenotypic plasticity vs. bet‐hedging) or instead are driven by geographic variation in genetic quality or parental effects.     

Rapid expansion of the cane toad (Bufo marinus) invasion front in tropical Australia

Abstract Cane toads (Bufo marinus) are large toxic anurans that have spread through much of tropical Australia since their introduction in 1935. Our surveys of the location of the toad invasion front in 2001 to 2005, and radiotracking of toads at the front near Darwin in 2005, reveal much faster westwards expansion than was recorded in earlier stages of toad invasion through Queensland. Since reaching the wet‐dry tropics of the Northern Territory, the toads have progressed an average of approximately 55 km year⁻¹ (mean rate of advance 264 m night⁻¹ along a frequently monitored 55‐km road transect during the wet season of 2004–2005). Radiotracking suggests that this displacement is due to rapid locomotion by free‐ranging toads rather than human‐assisted dispersal; individual toads frequently moved >200 m in a single night. One radiotracked toad moved >21 800 m in a 30‐day period; the fastest rate of movement yet recorded for any anuran. Daily displacements of radiotracked toads varied with time and local weather conditions, and were highest early in the wet season on warm, wet and windy nights. The accelerated rate of expansion of the front may reflect either, or both: (i) evolved changes in toads or (ii) that toads have now entered an environment more favourable to spread. This accelerated rate of expansion means that toads will reach the Western Australian border and their maximal range in northern Australia sooner than previously predicted.     

A ‘Goldilocks’ hypothesis for dispersal of biological control agents

The rate at which biological control agents disperse from release sites has important implications for their establishment and spread. Low rates of dispersal can yield spread that is too slow and may necessitate redistribution efforts for importation biological control and a high density of release sites for augmentation. Low dispersal rates may also lead to inbreeding at the site of release. On the other hand, high rates of dispersal can lead to Allee effects at the leading edge of the invasion front, potentially reducing the likelihood of establishment. Given these disadvantages associated with both low and high dispersal rates, we argue that intermediate rates of dispersal are likely to maximize the probability of establishment and appropriate spread for biological control agents released in the context of either importation or augmentative biological control. We consider this putative relationship a ‘Goldilocks hypothesis’ since it posits an optimum at intermediate values. In this review paper we begin by discussing the rationale for the Goldilocks hypothesis and then provide a case study from our work on importation biological control of the soybean aphid, Aphis glycines. Work on the soybean aphid parasitoid Binodoxys communis has shown that long-distance dispersal of immature parasitoids within winged migrating aphids is unlikely. This is likely good news for importation biological control because parasitoids dispersed in this manner would likely encounter crippling Allee effects. On the other hand, results from a field release study also suggest that female B. communis females (but not males) disperse actively from release sites. This female-biased dispersal may lead to strong mate-finding Allee effects and therefore may make establishment less likely.     

Seed dispersal of the non-native invasive tree <Emphasis Type="Italic">Ailanthus altissima</Emphasis> into contrasting environments

Ailanthus altissima has a long history of invasion in urban areas and is currently spreading into suburban and rural areas in the eastern U.S. The objectives of our study were to (1) determine whether A. altissima seed dispersal distance differed between populations on the edges of open fields and intact deciduous forest, and (2) determine whether dispersal differed for north and south winds. We also assessed the relationship between seed characteristics and distance from source populations in fields and forests, and whether seeds disperse at different rates throughout the dispersal season. Using two fields, two intact forest stands, and one partially harvested stand, we sampled the seed rain at 10 m intervals 100 m into each site from October to April 2002–2003. We compared seed density in field and intact forests using a three-way ANOVA with distance from source, wind direction, and environmental structure as independent variables. To assess the accuracy of common empirical dispersal models, mean seed density data at each site were fitted with alternative regression models. We found that mean seed dispersal distance depended on environmental structure and wind direction, a result driven in large part by dispersal at a single site where seed density did not decline with distance. The two alternative regression models fit each site’s dispersal curve equally well. More seeds were dispersed early than in mid- or late-season. Large, heavy seeds traveled as far as small light seeds. Turbulent winds appear to be necessary for seed release, as indicated by a wind tunnel experiment. A. altissima is able to disperse long distances into fields and into mature forests, and can reach canopy gaps and other suitable habitats at least 100 m from the forest edge. It is an effective disperser and can spread rapidly in fragmented landscapes where edges and other high light environments occur. These conditions are increasingly common throughout the eastern U.S. and in other temperate regions worldwide.     

Excluding access to invasion hubs can contain the spread of an invasive vertebrate

Many biological invasions do not occur as a gradual expansion along a continuous front, but result from the expansion of satellite populations that become established at 'invasion hubs'. Although theoretical studies indicate that targeting control efforts at invasion hubs can effectively contain the spread of invasions, few studies have demonstrated this in practice. In arid landscapes worldwide, humans have increased the availability of surface water by creating artificial water points (AWPs) such as troughs and dams for livestock. By experimentally excluding invasive cane toads (Bufo marinus) from AWP, we show that AWP provide a resource subsidy for non-arid-adapted toads and serve as dry season refuges and thus invasion hubs for cane toads in arid Australia. Using data on the distribution of permanent water in arid Australia and the dispersal potential of toads, we predict that systematically excluding toads from AWP would reduce the area of arid Australia across which toads are predicted to disperse and colonize under average climatic conditions by 38 per cent from 2,242,000 to 1,385,000 km(2). Our study shows how human modification of hydrological regimes can create a network of invasion hubs that facilitates a biological invasion, and confirms that targeted control at invasion hubs can reduce landscape connectivity to contain the spread of an invasive vertebrate.