Crystal Kelehear

Rhabdias pseudosphaerocephala infection in Bufo marinus: lung nematodes reduce viability of metamorph cane toads

Cane toads (Bufo marinus) were introduced to Australia in 1935 and have since spread widely over the continent, generating concern regarding ecological impacts on native predators. Most Australian cane toad populations are infected with lung nematodes Rhabdias pseudosphaerocephala, a parasite endemic to New World (native-range) cane toad populations; presumably introduced to Australia with its toad host. Considering the high intensities and prevalence reached by this parasite in Australian toad populations, and public ardour for developing a control plan for the invasive host species, the lack of experimental studies on this host-parasite system is surprising. To investigate the extent to which this lungworm influences cane toad viability, we experimentally infected metamorph toads (the smallest and presumably most vulnerable terrestrial phase of the anuran life cycle) with the helminth. Infected toads exhibited reduced survival and growth rates, impaired locomotor performance (both speed and endurance), and reduced prey intake. In summary, R. pseudosphaerocephala can substantially reduce the viability of metamorph cane toads.

Rapid evolution of parasite life history traits on an expanding range-edge

Parasites of invading species undergoing range advance may be exposed to powerful new selective forces. Low host density in range-edge populations hampers parasite transmission, requiring the parasite to survive longer periods in the external environment before encountering a potential host. These conditions should favour evolutionary shifts in offspring size to maximise parasite transmission. We conducted a common-garden experiment to compare life history traits among seven populations of the nematode lungworm (Rhabdias pseudosphaerocephala) spanning from the parasite population core to the expanding range-edge in invasive cane toads (Rhinella marina) in tropical Australia. Compared to conspecifics from the population core, nematodes from the range-edge exhibited larger eggs, larger free-living adults and larger infective larvae, and reduced age at maturity in parasitic adults. These results support a priori predictions regarding adaptive changes in offspring size as a function of invasion history, and suggest that parasite life history traits can evolve rapidly in response to the selective forces exerted by a biological invasion.

The early toad gets the worm: cane toads at an invasion front benefit from higher prey availability

In biological invasions, rates of range expansion tend to accelerate through time. What kind of benefits to more rapidly dispersing organisms might impose natural selection for faster rates of dispersal, and hence the evolution of range-edge acceleration? We can answer that question by comparing fitness-relevant ecological traits of individuals at the invasion front compared with conspecifics in the same area a few years post-invasion. In tropical Australia, the rate of invasion by cane toads (Rhinella marina) has increased substantially over recent decades, due to shifts in heritable traits. Our data on field-collected cane toads at a recently invaded site in the Australian wet-dry tropics span a 5-year period beginning with toad arrival. Compared with conspecifics that we monitored in the same sites post-invasion, toads in the invasion vanguard exhibited higher feeding rates, larger energy stores, better body condition and faster growth. Three processes may have contributed to this pattern: (i) higher prey availability at the front (perhaps due to reduced competition from conspecifics); (ii) the lack of viability-reducing parasites and pathogens in invasion-front toads; and (iii) distinctive (active, fast-growing) phenotypes of the invasion-front toads. Nutritional benefits to individuals in the invasion vanguard (whether because of higher prey availability, or lower pathogen levels) thus may have conferred a selective advantage to accelerated dispersal in this system.

Influence of lung parasites on the growth rates of free-ranging and captive adult cane toads

Many parasites affect the viability of their hosts, but detailed studies combining empirical data from both the field and the laboratory are limited. Consequently, the nature and magnitude of such effects are poorly known for many important host–parasite systems, including macroparasites of amphibians. We examined the effects of lungworm (Rhabdias pseudosphaerocephala) infections in cane toads (Bufo marinus) within their invasive Australian range. The host-specificity of this parasite suggests that it might serve as a biological control agent for toads in Australia, if infection proves to reduce toad viability. Mark–recapture studies in the field (near Darwin, Northern Territory) revealed lowered growth rates in infected adult toads when compared to uninfected toads, and a laboratory experiment confirmed causality: experimental infection with R. pseudosphaerocephala reduce toad growth rates. In combination with previous work on the current host–parasite system, it is now evident that nematode lungworms reduce the viability of both newly metamorphosed and adult cane toads, and do so in the field as well as in the laboratory. Rhabdias pseudosphaerocephala may be a valuable component of a biological control strategy for cane toads in Australia.

Corticosterone-immune interactions during captive stress in invading Australian cane toads (Rhinella marina).

Vertebrates cope with physiological challenges using two major mechanisms: the immune system and the hypothalamic pituitary-adrenal axis (e.g., the glucocorticoid stress response). Because the two systems are tightly integrated, we need simultaneous studies of both systems, in a range of species, to understand how vertebrates respond to novel challenges. To clarify how glucocorticoids modulate the amphibian immune system, we measured three immune parameters and plasma corticosterone (CORT), before and after inflicting a stressor (capture and captive confinement) on introduced cane toads (Rhinella marina) near their invasion front in Australia. Stress increased CORT levels, decreased complement lysis capacity, increased leukocyte oxidative burst, and did not change heterologous erythrocyte agglutination. The strength of the CORT response was positively correlated with leukocyte oxidative burst, and morphological features associated with invasiveness in cane toads (relative leg length) were correlated with stress responsiveness. No immune parameter that we measured was affected by a toads infection by a parasitic nematode (Rhabdias pseudosphaerocephala), but the CORT response was muted in infected versus uninfected toads. These results illustrate the complex immune-stress interactions in wild populations of a non-traditional model vertebrate species, and describe immune adaptations of an important invasive species.

Effects of Tail Autotomy on Anti-predator Behavior and Locomotor Performance in a Nocturnal Gecko

Abstract Caudal autotomy is widely employed by lizards to facilitate escape from predators. Despite conferring immediate short-term benefits, tail loss may involve substantial costs, including impaired locomotor performance, loss of energy reserves, and reduced survival during subsequent encounters with predators. We investigated whether tail autotomy influenced the running speeds and anti-predator behaviors of adult male Velvet Geckos, Oedura lesueurii. This nocturnal terrestrial gecko displays a range of anti-predator behaviors (tail waving and vibration, slow movement, and crypsis) in the presence of scent from the predatory Broad-headed Snake, Hoplocephalus bungaroides. Since tailless geckos cannot use tail displays to attract predatory strikes away from the torso, we hypothesized that tailless geckos would spend more time motionless in the presence of Broad-headed Snake scent. Sprint speeds of tailless and tailed Velvet Geckos were very similar over short (0.25 m) and longer distances (1 m). During locomotor trials, geckos frequently stopped along the racetrack, but tail autotomy did not affect the frequency of this behavior. Contrary to our predictions, tailless Velvet Geckos did not decrease their activity levels in the presence of Broad-headed Snake scent. Overall, our data support the hypothesis that the locomotor costs associated with tail autotomy are relatively minor in lizard species where the tail plays no functional role in locomotion.

Using Combined Morphological, Allometric and Molecular Approaches to Identify Species of the Genus Raillietiella (Pentastomida)

Taxonomic studies of parasites can be severely compromised if the host species affects parasite morphology; an uncritical analysis might recognize multiple taxa simply because of phenotypically plastic responses of parasite morphology to host physiology. Pentastomids of the genus Raillietiella are endoparasitic crustaceans primarily infecting the respiratory system of carnivorous reptiles, but also recorded from bufonid anurans. The delineation of pentastomids at the generic level is clear, but the taxonomic status of many species is not. We collected raillietiellids from lungs of the invasive cane toad (Rhinella marina), the invasive Asian house gecko (Hemidactylus frenatus), and a native tree frog (Litoria caerulea) in tropical Australia, and employed a combination of genetic analyses, and traditional and novel morphological methods to clarify their identity. Conventional analyses of parasite morphology (which focus on raw values of morphological traits) revealed two discrete clusters in terms of pentastome hook size, implying two different species of pentastomes: one from toads and a tree frog (Raillietiella indica) and another from lizards (Raillietiella frenatus). However, these clusters disappeared in allometric analyses that took pentastome body size into account, suggesting that only a single pentastome taxon may be involved. Our molecular data revealed no genetic differences between parasites in toads versus lizards, confirming that there was only one species: R. frenatus. This pentastome (previously known only from lizards) clearly is also capable of maturing in anurans. Our analyses show that the morphological features used in pentastomid taxonomy change as the parasite transitions through developmental stages in the definitive host. To facilitate valid descriptions of new species of pentastomes, future taxonomic work should include both morphological measurements (incorporating quantitative measures of body size and hook bluntness) and molecular data.

HOST-PARASITE RELATIONSHIPS DURING A BIOLOGIC INVASION: 75 YEARS POSTINVASION, CANE TOADS AND SYMPATRIC AUSTRALIAN FROGS RETAIN SEPARATE LUNGWORM FAUNAS

Invasive species may carry with them parasites from their native range, differing from parasite taxa found in the invaded range. Host switching by parasites (either from the invader to native fauna or from native fauna to the invader) may have important consequences for the viability of either type of host (e.g., their survivorship, fecundity, dispersal ability, or geographic distribution). Rhabdias pseudosphaerocephala (Nematoda) is a common parasite of cane toads (Rhinella marina) in the toad’s native range (South and Central America) and also in its introduced Australian range. This lungworm can depress host viability and is capable of infecting Australian frogs in laboratory trials. Despite syntopy between toads and frogs for up to 75 yr, our analyses, based on DNA sequence data of lungworms from 80 frogs and 56 toads, collected from 2008 to 2011, did not reveal any cases of host switching in nature: toads and native frogs retain entirely different lungworm faunas. All lungworms in cane toads were the South and Central American species Rhabdias pseudosphaerocephala, whereas Australian frogs contained at least four taxa (mostly undescribed and currently lumped under the name Rhabdias cf. hylae). General patterns of prevalence and intensity, based on the dissection of 1,315 frogs collected between 1989 and 2011 across the toads’ Australian range, show that these Australian endemic Rhabdias spp. are widely distributed geographically and across host taxa but are more common in some frog species (especially, large-bodied species) than they are in others.

NEMATODE LARVAE (ORDER SPIRURIDA) IN GASTRIC TISSUES OF AUSTRALIAN ANURANS: A COMPARISON BETWEEN THE INTRODUCED CANE TOAD AND SYMPATRIC NATIVE FROGS

The outcomes of host-parasite interactions depend heavily on the hosts immune response, which, in turn, is governed by previous interactions between the host and parasite, both over the hosts life time and over evolutionary time. In the case of species introductions, such as the cane toad (Bufo marinus) to Australia, parasites that are benign to native species of the introduced range may present a major challenge to the introduced species. Stomachs of introduced cane toads and seven species of sympatric native frogs were examined for parasites, and their pathology and biology were compared. Cane toads were host to eight species of third-stage spirurid larvae, six of which also occurred in the stomach wall of four native frog species. In general, encysted nematode larvae attained higher prevalence and species richness in introduced cane toads than in sympatric native frogs. This trend was largely explained by differences in body sizes: larger anurans were more likely to possess infections, and cane toads are inherently larger than native frogs. Encysted larvae in cane toad stomachs provoked a marked pathologic response. All larvae (physalopterine and Physocephalus spp.) were surrounded by concentric layers of dense, fibrous tissue, with considerable cellular infiltration characterized by lymphocytes and polymorphs. Many cysts were invaded by cells and exudate, which, in more advanced cases, became calcified. Some larvae appeared viable; most were in various stages of destruction, and some smaller Physocephalus spp. were mummified. Conversely, pathologic response observed in native frogs was minimal, with little fibrotic reaction surrounding the cysts, and no cellular infiltration. Presumably, the contrast in pathology between introduced and native hosts reflects the long evolutionary association between these nematode larvae and native frogs, whereas the recent exposure of introduced toads to these helminths provokes a severe reaction.

Seasonal dynamics of the lungworm, Rhabdias pseudosphaerocephala, in recently colonised cane toad (Rhinella marina) populations in tropical Australia.

The impact of parasites on host populations depend upon parasite prevalence and intensity. Understanding how infection dynamics change through time following a host populations initial exposure to the parasite is fundamental to host-parasite biology. We studied an invasive host (the cane toad, Rhinella marina) currently undergoing range expansion - a process through which this hosts range is expanding faster than that of its lung parasites (the nematode, Rhabdias pseudosphaerocephala), such that hosts at the expanding range edge remain parasite-free for several years. It was predicted that parasite intensity and prevalence would be affected by host characteristics (e.g., size, sex), environmental conditions (e.g., seasons, habitat type), and time since parasite arrival in the newly established invading host population. Over 2,400 cane toads were sampled at 10 sites in recently established toad populations in the highly seasonal monsoonal tropics of northern Australia. The sampling spanned 14 consecutive 3 month seasons commencing in the early stages of lungworm establishment in those toad populations. Both parasite prevalence and intensity increased with host body size but were unaffected by host sex. Prevalence and intensity were highest during drier times of year and in drier habitats (i.e., sites lacking permanent waterbodies). These changes in parasite prevalence may reflect a trend for saturated soil to reduce parasite survival during the free-living infective stage, and to allow anuran hosts to disperse widely (thus reducing the transfer of directly transmitted parasites between hosts). Conversely, dry conditions induce toads to aggregate in moist dry-season refugia where conditions may be more conducive to direct transmission of infective parasitic larvae between hosts.