Desiccation risk drives the spatial ecology of an invasive anuran (Rhinella marina) in the Australian semi-desert

Some invasive species flourish in places that impose challenges very different from those faced in their native geographic ranges. Cane toads (Rhinella marina) are native to tropical and subtropical habitats of South and Central America, but have colonised extremely arid regions over the course of their Australian invasion. We radio-tracked 44 adult cane toads at a semi-arid invasion front to investigate how this invasive anuran has managed to expand its geographic range into arid areas that lie outside of its native climatic niche. As predicted from their low physiological control over rates of evaporative water loss, toads selected diurnal shelter sites that were consistently cooler and damper (and thus, conferred lower water loss rates) than nearby random sites. Desiccation risk also had a profound influence on rates of daily movement. Under wet conditions, toads that were far from water moved further between shelter sites than did conspecifics that remained close to water, presumably in an attempt to reach permanent water sources. However, this relationship was reversed under dry conditions, such that only toads that were close to permanent water bodies made substantial daily movements. Toads that were far from water bodies also travelled along straighter paths than did conspecifics that generally remained close to water. Thus, behavioural flexibility--in particular, an ability to exploit spatial and temporal heterogeneity in the availability of moist conditions--has allowed this invasive anuran to successfully colonize arid habitats in Australia. This finding illustrates that risk assessment protocols need to recognise that under some circumstances an introduced species may be able to thrive in conditions far removed from any that it experiences in its native range.     

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 toad's 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.     

Myrmecochory in some plants (F. chenopodiaceae) of the Australian arid zone

Summary Several common plants (Chenopodiaceae) of the Australian arid zone produce diaspores that bear small and inconspicuous food bodies and are adapted for dispersal by ants. For these species, myrmecochory probably represents an adaptation for highly directional dispersal of diaspores to favorable microsites where nutrients are concentrated and possibly more accessible. Dispersal of diaspores by ants can have a pronounced effect on plant dispersion. In habitats characterized by red, crusty alluvial loam soils, myrmecochorous species grow almost exclusively on ant mounds; these same species grow in relatively continuous stands in sandy soil habitats. The flora of the Australia arid zone may contain many plant species that are adapted to use ants as dispersal agents. We consider several factors that may have promoted or facilitated the evolution of myrmecochory in arid zone plants.     

Morphological differentiation among populations of Rhinella marina (Amphibia: Anura) in western Mexico

Conspecific populations inhabiting different environments may exhibit morphological differences, potentially reflecting differential local adaptation. In anuran amphibians, morphology of the pelvis and hindlimbs may often experience strong selection due to effects on locomotion. In this study, we used the cane toad Rhinella marina to test the hypothesis that populations experiencing a higher abundance of predators should suffer higher mortality rates and exhibit morphological traits associated with enhanced locomotor performance (narrower pelvis and head, longer pelvis and hindlimbs, shorter presacral vertebral column). We investigated inter-population variation in survival rate, abundance of predators, and body shape across five populations in rivers in western Mexico. We conducted (1) mark-recapture experiments to calculate survival rates, (2) linear transects with point counts to estimate abundance of predatory spiders, snakes, and birds, and (3) geometric morphometric analyses to investigate body shape variation. We found significant differences among populations in survival rates, abundance of predators, and body shape. However, these three variables were not necessarily inter-related. Increased predator abundance did not result in decreased survival rates, suggesting other causes of mortality affect these populations. While some morphological differences supported our predictions (trend for longer pelvis, shorter presacral vertebral column, and narrower head in sites with increased abundance of spiders and snakes), other aspects of morphology did not. We discuss alternative explanations for the lack of clear associations between predation, survival, and morphology.     

Food of the zebra finch (Poephila guttata), and an examination of granivory in birds of the Australian arid zone

Birds are important granivores in the Australian arid zone, and this paper reviews their role by assembling available data on diet and habitat selection of the granivorous species occurring in the region. Paucity of dietary information is alleviated by a study of the food of the zebra finch (Poephila guttata) at two sites in the eastern arid zone. Zebra finches subsisted entirely on grass seeds of a relatively narrow specific range; 17 classes of seeds (at least 19 species) were eaten, but one class dominated the diet at each study site and only five classes (probably six species) were significant overall. Comparative information concerning granivorous species- suggested that the seeds of grasses and shrubs are of most importance in diets, that larger species tended to eat larger seeds from a wider variety of plants because of the addition of shrub species to the diet, and that Acacia shrublands contained most species. Characteristics of the arid zone that are of particular importance to granivorous birds appear to be the abundance of grasses and the patchy and erratic nature of the rainfall.     

Larger Body Size at Metamorphosis Enhances Survival,Growth and Performance of Young Cane Toads (Rhinella marina)

Body size at metamorphosis is a key trait in species (such as many anurans) with biphasic life-histories. Experimental studies have shown that metamorph size is highly plastic, depending upon larval density and environmental conditions (e.g. temperature, food supply, water quality, chemical cues from conspecifics, predators and competitors). To test the hypothesis that this developmental plasticity is adaptive, or to determine if inducing plasticity can be used to control an invasive species, we need to know whether or not a metamorphosing anuran’s body size influences its subsequent viability. For logistical reasons, there are few data on this topic under field conditions. We studied cane toads (Rhinella marina) within their invasive Australian range. Metamorph body size is highly plastic in this species, and our laboratory studies showed that larger metamorphs had better locomotor performance (both on land and in the water), and were more adept at catching and consuming prey. In mark-recapture trials in outdoor enclosures, larger body size enhanced metamorph survival and growth rate under some seasonal conditions. Larger metamorphs maintained their size advantage over smaller siblings for at least a month. Our data support the critical but rarely-tested assumption that all else being equal, larger body size at metamorphosis is likely to enhance an individual’s long term viability. Thus, manipulations to reduce body size at metamorphosis in cane toads may help to reduce the ecological impact of this invasive species.     

Patterns of Genetic Variability in Island Populations of the Cane Toad (Rhinella marina) from the Mouth of the Amazon

The Amazonian coast has several unique geological characteristics resulting from the interaction between drainage pattern of the Amazon River and the Atlantic Ocean. It is one of the most extensive and sedimentologically dynamic regions of the world, with a large number of continental islands mostly formed less than 10,000 years ago. The natural distribution of the cane toad (Rhinella marina), one of the world’s most successful invasive species, in this complex Amazonian system provides an intriguing model for the investigation of the effects of isolation or the combined effects of isolation and habitat dynamic changes on patterns of genetic variability and population differentiation. We used nine fast-evolving microsatellite loci to contrast patterns of genetic variability in six coastal (three mainlands and three islands) populations of the cane toad near the mouth of the Amazon River. Results from Bayesian multilocus clustering approach and Discriminant Analyses of Principal Component were congruent in showing that each island population was genetically differentiated from the mainland populations. All F_ST values obtained from all pairwise comparisons were significant, ranging from 0.048 to 0.186. Estimates of both recent and historical gene flow were not significantly different from zero across all population pairs, except the two mainland populations inhabiting continuous habitats. Patterns of population differentiation, with a high level of population substructure and absence/restricted gene flow, suggested that island populations of R. marina are likely isolated since the Holocene sea-level rise. However, considering the similar levels of genetic variability found in both island and mainland populations, it is reliable to assume that they were also isolated for longer periods. Given the genetic uniqueness of each cane toad population, together with the high natural vulnerability of the coastal regions and intense human pressures, we suggest that these populations should be treated as discrete units for conservation management purposes.     

Phylogeny and biogeography of the Rhinella marina species complex (Amphibia,Bufonidae) revisited: implications for Neotropical diversification hypotheses

Vallinoto, M., Sequeira, F., Sodré, D., Bernardi, J. A. R., Sampaio, I. & Schneider, H. (2009). Phylogeny and biogeography of the Rhinella marina species complex (Amphibia, Bufonidae) revisited: implications for Neotropical diversification hypotheses. —Zoologica Scripta, 39, 128–140. A number of distinct hypotheses have been proposed to account for the origin of the considerable biological diversity found in the Neotropics, which is still a matter of intense debate. Here, we conducted a phylogenetic analysis of the Rhinella marina complex, a group of species widely distributed in Central and South America, combining published data with new sequences of three mtDNA genes (12S, 16S and cyt b) in order to clarify the evolutionary relationships and biogeographical history of the group. We included eight of the ten currently recognized R. marina group species and several outgroups. Maximum parsimony, maximum likelihood, and Bayesian inference analyses produced similar topologies, with two well‐supported main clades, each characterized by a deep subdivision. One of these major clades includes the samples of R. marina from Central America and Ecuador (west of the Andes), whereas the other comprises the remaining species of the group and samples of R. marina from the Amazon basin and other areas east of the Andes. A Bayesian coalescent‐based method (BEAST) dated the divergence between the two major clades, and between the Central American and Ecuadorian clades to the Miocene, matching the timing of other Central‐South American faunal divergences. Taken together, the results highlight the importance of Tertiary events such as the Pebas/marine incursions into the Amazon basin and Andean uplift for the diversification and historical biogeography of R. marina, making such taxa paraphyletic, and provide new perspectives on the debate on its species status.     

A new species of Mesocoelium (Digenea: Mesocoeliidae) found in Rhinella marina (Amphibia: Bufonidae) from Brazilian Amazonia

Mesocoelium lanfrediaesp. nov. (Digenea: Mesocoeliidae) inhabits the small intestine of Rhinella marina (Amphibia: Bufonidae) and is described here, with illustrations provided by light, scanning electron microscopy and molecular approachs. M. lanfrediae sp. nov. presents the typical characteristics of the genus, but is morphometrically and morphologically different from the species described previously. The main diagnostic characteristics of M. lanfrediae sp. nov. are (i) seven pairs of regularly-distributed spherical papillae on the oral sucker, (ii) ventral sucker outlined by four pairs of papillae distributed in a uniform pattern and interspersed with numerous spines, which are larger at the posterior margin and (iii) small, rounded tegumentary papillae around the opening of the oral sucker, which are morphologically different from those of the oral sucker itself, some of which are randomly disposed in the ventrolateral tegumentary region of the anterior third of the body. Addionally, based on SSU rDNA, a phylogenetic analysis including Brachycoeliidae and Mesocoeliidae taxa available on GenBank established the close relationship between M. lanfrediae sp. nov. and Mesocoelium sp.     

Pectoral girdle movements and the role of the glenohumeral joint during landing in the toad, Rhinella marina (Linnaeus, 1758)

Compared to anurans from other families, landings of toads (Bufonidae) during saltation appear well coordinated and the initial landing impact is absorbed exclusively by the forelimbs. Although the forelimbs and particularly the pectoral girdle have been suggested to be important for shock absorption, the functional roles of its various elements have not been evaluated in detail. This study addresses open questions regarding the kinematics of the forelimbs during landing in Rhinella marina using X-ray reconstruction of moving morphology and scientific rotoscoping. The kinematic analysis clearly showed that in addition to motions in the shoulder and elbow joints, substantial movements of the pectoral girdle in toto as well as of its elements relative to each other do occur during landing. The pectoral girdle showed first and foremost rotations about its latero-lateral axis as well as dorso-ventral translations relative to the spine. Our results quantify the extent of flexion and extension in the suprascapula-scapular synchondrosis during landing. Forelimb kinematics in R. marina differed from that of other anurans in starting elbow extension relatively early during the landing process, which likely prevents the chest from contacting the ground. Furthermore, the animal regains an upright and ready-to-hop-again position quickly and the recovery phase is short compared to other anurans. Humeral kinematics and anatomy confirm that the glenohumeral interlocking mechanism guides the humerus during the initial landing phase. Cranio-ventral ridges on the humeral head and the paraglenoid cartilage interlock in anteverted and slightly retroverted humeral positions. This occurs at the beginning of the landing. When interlocked, adduction/abduction as well as long-axis rotation of the humerus are restricted. During the course of landing, the humerus retroverts and is gradually freed from interlocking restrictions due to a smoother relief at the caudal aspect of the humeral head.     

Effects of spines and thorns on Australian arid zone herbivores of different body masses

Summary We investigated the effects of thorns and spines on the feeding of 5 herbivore species in arid Australia. The herbivores were the rabbit (Oryctolagus cuniculus), euro kangaroo (Macropus robustus), red kangaroo (Macropus rufus), sheep (Ovis aries), and cattle (Bos taurus). Five woody plants without spines or thorns and 6 woody plants with thorns were included in the study. The spines and thorns were not found to affect the herbivores' rates of feeding (items ingested/min), but they did reduce the herbivores' rates of biomass ingestion (g-dry/item). The reduction in biomass ingested occurred in two ways: at a given diameter, twigs with spines and thorns had less mass than undefended plants, and the herbivores consumed twigs with smaller diameters on plants with spines and thorns. The relative importance of the two ways that twigs with spines and thorns provided less biomass varied with herbivore body mass. Reduced twig mass was more important for small herbivores, while large herbivores selected smaller diameters. The effectiveness of spines and thorns as anti-herbivore defenses did not vary with the evolutionary history of the herbivores (i.e. native vs. introduced). Spines and thorns mainly affected the herbivores' selection of maximum twig sizes (reducing diameter and mass), but the minimum twig sizes selected were also reduced.     

The life stages and population dynamics of an arid zone scorpion Urodacus yaschenkoi (Birula 1903)

The arid zone scorpion Urodacus yaschenkoi (Birula 1903) is shown to have six instars. Instars can be recognized by measuring the claws and the carapace plus first five tail segments. A population study, carried out at Coombah, NSW, showed that the life history consisted of mating in September–October, 18 month gestation, birth in February-March, moult to second instar March-April and annual moults to sixth instar in December–February. The minimum generation time was 6 y, and the population appeared to be stable. The calendar of catches method was used to determine the population size (about 400 animals in 2240 m²) but required some extra assumptions to cope with loss of marks from individuals when they moulted.     

Fish larvae, growth and biomass relationships in an Australian arid zone river: links between floodplains and waterholes

1. Floodplain inundation provides many benefits to fish assemblages of floodplain river systems, particularly those with a predictable annual flood pulse that drives yearly peaks in fish production. In arid‐zone rivers, hydrological patterns are highly variable and the influence of irregular floods on fish production and floodplain energy subsidies may be less clear‐cut. To investigate the importance of floodplain inundation to a dryland river fish assemblage, we sampled fish life stages on the floodplain of Cooper Creek, an Australian arid‐zone river. Sampling was focused around Windorah during a major flood in January 2004 and in isolated waterholes in March 2004 following flood drawdown. 2. Of the 12 native species known to occur in this region, 11 were present on the floodplain, and all were represented by at least two of three life‐stages – larvae, juveniles or adult fish. Late stage larvae of six fish species were found on the floodplain. There were site‐specific differences in larval species assemblages, individual species abundances and larval distribution patterns among floodplain sites. 3. Significant growth was evident on the floodplain, particularly by larval and juvenile fish, reflecting the combination of high water temperatures and shallow, food rich habitats provided by the relatively flat floodplain. 4. Low variation in biomass, species richness and presence/absence of juvenile and adult fish across four floodplain sites indicates consistently high fish productivity across an extensive area. 5. Similarities and differences in fish biomass between the floodplain and isolated post‐flood waterholes suggest high rates of biomass transfer (involving the most abundant species) into local waterholes and, potentially, biomass transfer by some species to other waterholes in the catchment during floodplain inundation and after floods recede. 6. The high concentration of fish on this shallow floodplain suggests it could be a key area of high fish production that drives a significant proportion of waterhole productivity in the vicinity. The Windorah floodplain provides favourable conditions necessary for the spawning of some species and juvenile recruitment of the majority of species. It is also appears to be a significant conduit for the movements of fish that underpin high genetic similarity, hence population mixing, of many species throughout the Cooper Creek catchment. The high floodplain fish production in turn provides a significant energy subsidy to waterholes after floodwaters recede. 7. The identification of key sites of high fish production, such as the Windorah floodplain, may be important from a conservation perspective. Key management principles should be: maintenance of the natural flooding regime; identification of the most productive floodplain areas; and maintenance of their connectivity to anastomosing river channels and the remnant aquatic habitats that ultimately sustain this fish assemblage through long‐term dry/drought and flood cycles.     

Birth of a biome: insights into the assembly and maintenance of the Australian arid zone biota

The integration of phylogenetics, phylogeography and palaeoenvironmental studies is providing major insights into the historical forces that have shaped the Earth's biomes. Yet our present view is biased towards arctic and temperate/tropical forest regions, with very little focus on the extensive arid regions of the planet. The Australian arid zone is one of the largest desert landform systems in the world, with a unique, diverse and relatively well-studied biota. With foci on palaeoenvironmental and molecular data, we here review what is known about the assembly and maintenance of this biome in the context of its physical history, and in comparison with other mesic biomes. Aridification of Australia began in the Mid-Miocene, around 15 million years, but fully arid landforms in central Australia appeared much later, around 1-4 million years. Dated molecular phylogenies of diverse taxa show the deepest divergences of arid-adapted taxa from the Mid-Miocene, consistent with the onset of desiccation. There is evidence of arid-adapted taxa evolving from mesic-adapted ancestors, and also of speciation within the arid zone. There is no evidence for an increase in speciation rate during the Pleistocene, and most arid-zone species lineages date to the Pliocene or earlier. The last 0.8 million years have seen major fluctuations of the arid zone, with large areas covered by mobile sand dunes during glacial maxima. Some large, vagile taxa show patterns of recent expansion and migration throughout the arid zone, in parallel with the ice sheet-imposed range shifts in Northern Hemisphere taxa. Yet other taxa show high lineage diversity and strong phylogeographical structure, indicating persistence in multiple localised refugia over several glacial maxima. Similar to the Northern Hemisphere, Pleistocene range shifts have produced suture zones, creating the opportunity for diversification and speciation through hybridisation, polyploidy and parthenogenesis. This review highlights the opportunities that development of arid conditions provides for rapid and diverse evolutionary radiations, and re-enforces the emerging view that Pleistocene environmental change can have diverse impacts on genetic structure and diversity in different biomes. There is a clear need for more detailed and targeted phylogeographical studies of Australia's arid biota and we suggest a framework and a set of a priori hypotheses by which to proceed.     

Comparative ecophysiology of the harmful alga Chattonella marina (Raphidophyceae) form South Australian and Japanese waters

The raphidophyte flagellate Chattonella marina was successfully cultured from Boston Bay (South Australia), coincident with mass mortality of farmed bluefin tuna (Thunnus maccoyii) in April 1996. Grown under laboratory conditions at 150 mol m^-2 s^-1 irradiance, optimal growth (>0.5 day^-1) occurred at a temperature of 25C and a salinity of 30 p.s.u., but good growth (>0.3 day^-1) also occurred between a temperature of 10 and 30°C and at a salinity of 15-45 p.s.u. However, cultures grow much faster at an irradiance of 450 mol m^-2 s^-1 (1.08 day^-1). While Australian C.marina had similar temperature and salinity requirements as well-studied Japanese cultures from the Seto Inland Sea, the Australian strains exhibited a light saturation level for growth four times higher than that reported from Japan (150 mol m^-2 s^-1). An adaptation to higher light intensities was reflected in higher concentrations of microsporine-like amino acids in the Australian strains. The different light adaptation phenotypes were still apparent after long-term culturing under similar physiological conditions. Potential growth habitats for this ichthyotoxic flagellate in the Australian region and implications for finfish aquaculture industries are discussed.      

Rhabdias paraensis sp. nov.: a parasite of the lungs of Rhinella marina (Amphibia: Bufonidae) from Brazilian Amazonia

The nematode parasites of Rhinella marina include species of the genus Rhabdias (Rhabdiasidae: Rhabditoidea). The present study describes Rhabdias paraensis sp. nov., which parasitizes the lungs of R. marina in Brazilian Amazonia. Of the more than 70 known species of this genus, 18 are parasites of bufonids, of which, eight are Neotropical. The new species described here is similar to Rhabdias alabialis in the absence of lips is different by the presence of conspicuous cephalic papillae. We describe details of the four rows of pores, which are distributed equally along the whole of the length of the body and connected with hypodermal cells, using histology and scanning electron microscopy. Other histological aspects of the internal structure of this nematode are also described.     

Uncovering cryptic evolutionary diversity in extant and extinct populations of the southern Australian arid zone Western and Thick-billed Grasswrens (Passeriformes: Maluridae: Amytornis)

The Western and Thick-billed Grasswrens (Aves: Passeriformes: Maluridae: Amytornis textilis and Amytornis modestus, respectively) exemplify issues surrounding the evolution, biogeography and conservation of Australia’s arid and semi-arid zone fauna. The two species together have historically occurred across much of southern Australia. They showed high intraspecific taxonomic diversity and short range endemism but suffered high rates of recent anthropogenic extinction. Of 11 named and 1 un-named subspecies, 5 are extinct and 3 are vulnerable or critically endangered. To clarify taxonomic issues, and to understand their pre-extinction phylogeography and identify extant populations and taxa of conservation value, we sequenced ~1,000 bp of the mtDNA ND2 gene from all extant populations and all but one extinct population. We confirmed reciprocal monophyly of A. modestus and A. textilis and identified strong phylogeographic structure associated with morphological divergence within each species. Populations of A. t. myall at the western edge of their range in South Australia may preserve “ghost” lineages of extinct subspecies from Western Australia as a result of ancient gene flow. Our results support recent taxonomic revisions, and highlight the critical importance of including samples of extirpated populations and extinct species to fully understand and interpret extant diversity. Conservation and management plans should recognise and seek to preserve the unique evolutionary diversity present in surviving populations.