The effect of salt dosing for chytrid mitigation on tadpoles of a threatened frog, Litoria aurea.

The novel fungal pathogen Batrachochytrium dendrobatidis (chytrid) is one of the greatest threats to amphibians worldwide. Small increases in water salinity (up to ca. 4 ppt) have been shown to limit chytrid transmission between frogs, potentially providing a way to create environmental refugia to reduce its impact at a landscape scale. However, the effect of increasing water salinity on tadpoles, a life stage confined to water, is highly variable. Increased water salinity can lead to reduced size and altered growth patterns in some species, with flow-on effects to vital rates such as survival and reproduction. It is thus important to assess potential trade-offs caused by increasing salinity as a tool to mitigate chytrid in susceptible frogs. We conducted laboratory experiments to examine the effects of salinity on the survival and development of tadpoles of a threatened frog (Litoria aurea), previously demonstrated as a suitable candidate for trialling landscape manipulations to mitigate chytrid. We exposed tadpoles to salinity ranging from 1 to 6 ppt and measured survival, time to metamorphosis, body mass and locomotor performance of post-metamorphic frogs as a measure of fitness. Survival and time to metamorphosis did not differ between salinity treatments or controls reared in rainwater. Body mass was positively associated with increasing salinity in the first 14 days. Juvenile frogs from three salinity treatments also showed the same or better locomotor performance compared to rainwater controls, confirming that environmental salinity may influence life history traits in the larval stage, potentially as a hormetic response. Our research suggests that salt concentrations in the range previously shown to improve survival of frogs in the presence of chytrid are unlikely to impact larval development of our candidate threatened species. Our study lends support to the idea of manipulating salinity to create environmental refugia from chytrid for at least some salt-tolerant species.

Increased rates of dispersal of free-ranging cane toads (Rhinella marina) during their global invasion.

Invasions often accelerate through time, as dispersal-enhancing traits accumulate at the expanding range edge. How does the dispersal behaviour of individual organisms shift to increase rates of population spread? We collate data from 44 radio-tracking studies (in total, of 650 animals) of cane toads (Rhinella marina) to quantify distances moved per day, and the frequency of displacement in their native range (French Guiana) and two invaded areas (Hawai'i and Australia). We show that toads in their native-range, Hawai'i and eastern Australia are relatively sedentary, while toads dispersing across tropical Australia increased their daily distances travelled from 20 to 200 m per day. That increase reflects an increasing propensity to change diurnal retreat sites every day, as well as to move further during each nocturnal displacement. Daily changes in retreat site evolved earlier than did changes in distances moved per night, indicating a breakdown in philopatry before other movement behaviours were optimised to maximise dispersal.

Body shape and food habits of South American goo-eater snakes of the genus Sibynomorphus

Snakes of the tribe Dipsadini feed mostly on annelids, slugs, and snails. Some species that feed exclusively on snails are able to de-shell their prey prior ingestion. On the basis of dissection of preserved specimens from museums, we report the dietary habits of three species of Sibynomorphus from Brazil. Eighteen to 26% of the snakes had stomach contents, varying from 1-8 items, and the number of prey was not correlated with snake size. Prey mass was positively correlated with snake mass, but relative prey mass decreased with increasing snake size. Prey mass represented less than 5% of the predator mass for all species. Sibynomorphus neuwiedi and S. mikanii only had Veronicellidae slugs in their digestive tract, whereas S. ventrimaculatus also included snails in their diet. Sibynomorphus mikanii ingested most prey rear-first, but there was no difference in direction of prey ingestion by the other two species. Snake morphology differed among species and provided insights into habitat use and feeding habits. Sibynomorphus neuwiedi was the largest species and had the longest tail. Its eyes were also larger than those of S. mikanii, which, together with tail size, suggests more arboreal habits. Sibynomorphus ventrimaculatus had the largest head relatie to the body, which might facilitate ingestion of snails. In summary, the three species of Sibynomporphus are slug specialists. Like other goo-eaters, these snakes feed on very small and low caloric prey, which might require them to feed frequently. This hypothesis is supported by the larger number of prey ingested by these snakes compared to non-goo-eater species of Dipsadini.

Body shape and food habits of South American goo-eater snakes of the genus Sibynomorphus

Snakes of the tribe Dipsadini feed mostly on annelids, slugs, and snails. Some species that feed exclusively on snails are able to de-shell their prey prior ingestion. On the basis of dissection of preserved specimens from museums, we report the dietary habits of three species of Sibynomorphus from Brazil. Eighteen to 26% of the snakes had stomach contents, varying from 1-8 items, and the number of prey was not correlated with snake size. Prey mass was positively correlated with snake mass, but relative prey mass decreased with increasing snake size. Prey mass represented less than 5% of the predator mass for all species. Sibynomorphus neuwiedi and S. mikanii only had Veronicellidae slugs in their digestive tract, whereas S. ventrimaculatus also included snails in their diet. Sibynomorphus mikanii ingested most prey rear-first, but there was no difference in direction of prey ingestion by the other two species. Snake morphology differed among species and provided insights into habitat use and feeding habits. Sibynomorphus neuwiedi was the largest species and had the longest tail. Its eyes were also larger than those of S. mikanii, which, together with tail size, suggests more arboreal habits. Sibynomorphus ventrimaculatus had the largest head relatie to the body, which might facilitate ingestion of snails. In summary, the three species of Sibynomporphus are slug specialists. Like other goo-eaters, these snakes feed on very small and low caloric prey, which might require them to feed frequently. This hypothesis is supported by the larger number of prey ingested by these snakes compared to non-goo-eater species of Dipsadini.

Quantifying anuran microhabitat use to infer the potential for parasite transmission between invasive cane toads and two species of Australian native frogs.

Parasites that are carried by invasive species can infect native taxa, with devastating consequences. In Australia, invading cane toads (Rhinella marina) carry lungworm parasites (Rhabdias pseudosphaerocephala) that (based on previous laboratory studies) can infect native treefrogs (Litoria caerulea and L. splendida). To assess the potential of parasite transmission from the invader to the native species (and from one infected native frog to another), we used surveys and radiotelemetry to quantify anuran microhabitat use, and proximity to other anurans, in two sites in tropical Australia. Unsurprisingly, treefrogs spent much of their time off the ground (especially by day, and in undisturbed forests) but terrestrial activity was common at night (especially in anthropogenically modified habitats). Microhabitat overlap between cane toads and frogs was generally low, except at night in disturbed areas, whereas overlap between the two frog species was high. The situations of highest overlap, and hence with the greatest danger of parasite transmission, involve aggregations of frogs within crevices by day, and use of open ground by all three anuran species at night. Overall, microhabitat divergence between toads and frogs should reduce, but not eliminate, the transmission of lungworms from invasive toads to vulnerable native frogs.

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 population's 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 host's 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.

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.

Patterns of interspecific variation in the heart rates of embryonic reptiles.

New non-invasive technologies allow direct measurement of heart rates (and thus, developmental rates) of embryos. We applied these methods to a diverse array of oviparous reptiles (24 species of lizards, 18 snakes, 11 turtles, 1 crocodilian), to identify general influences on cardiac rates during embryogenesis. Heart rates increased with ambient temperature in all lineages, but (at the same temperature) were faster in lizards and turtles than in snakes and crocodilians. We analysed these data within a phylogenetic framework. Embryonic heart rates were faster in species with smaller adult sizes, smaller egg sizes, and shorter incubation periods. Phylogenetic changes in heart rates were negatively correlated with concurrent changes in adult body mass and residual incubation period among the lizards, snakes (especially within pythons) and crocodilians. The total number of embryonic heart beats between oviposition and hatching was lower in squamates than in turtles or the crocodilian. Within squamates, embryonic iguanians and gekkonids required more heartbeats to complete development than did embryos of the other squamate families that we tested. These differences plausibly reflect phylogenetic divergence in the proportion of embryogenesis completed before versus after laying.

The effects of experimentally infecting Australian tree frogs with lungworms (Rhabdias pseudosphaerocephala) from invasive cane toads.

Invasive species may transmit novel pathogens to native taxa, and lacking a history of coevolutionary interactions with the pathogen, the new hosts may be severely affected. Cane toads (Rhinella marina) were introduced to Australia in 1935, bringing with them a lungworm (Rhabdias pseudosphaerocephala) not found in Australian frogs. Previous studies suggest that most frog species are unaffected by this parasite, but one tree-frog (Litoria caerulea) can harbour high numbers of lungworm. More detailed laboratory studies confirm and extend the earlier results on L. caerulea and show that Rhabdias infection severely depresses the viability of metamorphs of an allied tree-frog species, Litoria splendida. Parasitic larvae infected both of these two closely related tree-frog species, but the two anurans differed in the consequences of infection. Parasitism reduced the survivorship of L. splendida and the stamina of both species. Lungworms did not consistently reduce growth rates or affect heart rates in either tree-frog species. Although L. splendida is potentially vulnerable to the arrival of toad-transported lungworms, rates of host-switching may be reduced by low levels of habitat overlap between the frogs (which are rock-dwelling and arboreal) and the toads (which are terrestrial and most abundant in disturbed habitats).

Infection dynamics of the lungworm Rhabdias pseudosphaerocephala in its natural host, the cane toad (Bufo marinus), and in novel hosts (native Australian frogs).

Host-parasite systems have often evolved over time, such that infection dynamics may become greatly modified from the time of initial contact of the host with the parasite. Biological invasions may be useful to clarify processes in the initial contact of hosts with parasites, and allow us to compare parasite uptake between the ancestral (coevolved) host and novel (noncoevolved) hosts. Cane toads (Bufo marinus) are spreading rapidly through tropical Australia, carrying with them a nematode lungworm (Rhabdias pseudosphaerocephala) congeneric with those found in Australian frogs. We investigated the dynamics of infections of the toad parasite by conducting histologic examinations of cane toads and three native Australian frogs (Litoria dahlii, Litoria nasuta, and Opisthodon ornatus) at 2, 6, and 10 days after experimental exposure to the toad lungworm. More worms were found in toads than in frogs, especially at longer periods postexposure. In toads, the infective larvae entered the skin and muscles within 2 days postexposure, passed into the coelom in 6 days, and reached the lungs at 10 days. In frogs, larvae were found in many organs rather than migrating to consistent target tissues; a few larvae reached the lungs of L. dahlii. Migratory larvae caused increasing inflammation (primarily granulomatous admixed with granulocytes then lymphocytes) through time, especially in frogs. Evolution has resulted in an enhanced ability of the lungworm to locate the target organ (the lungs) of the toad, and an increase in rates of parasite survival within this host.

Reproductive biology and food habits of Pseudoboa nigra (Serpentes Dipsadidae) from the Brazilian cerrado / Biologia reprodutiva e hábitos alimentares de Pseudoboa nigra (Serpentes Dipsadidae) do cerrado brasileiro

Reproductive biology and food habits of Pseudoboa nigra (Serpentes: Dpsadidae) from the Brazilian cerrado. Herein we provide data on body size, sexual size dimorphism, reproductive cycle, and food habits of the pseudoboini snake Pseudoboa nigra, wich is dissections of 147 preserved specimens, it is shown that femmales attain, and mature at, larger body sizes than males. There is no significant sexual dimorphism in head lenght, but males have longer tails to their body sizes. Vitellogenesis, egg-laying, and sperm production occur throughout the year, but males do not exhibit long-term sperm storage. The main prey of P. nigra is lizards; there is no evidence of ontogenetic change or sex differences in the diet of this species.

Biologia reprodutiva e hábitos alimentares de Pseudoboa nigra (Serpentes: Dipsadidae) do cerrado brasileiro. Neste trabalho fornecemos informações sobre tamanho corporal, dimorfismo sexual, ciclo reprodutivo e hábitos alimentares da serpente Pseudoboini Pseudoboa nigra, que corre no domínio do Cerrado na região Central da América do Sul. Com base na dissecção de 147 espécimes preservados, mostramos que as fêmeas são em média maiores e atinguem maturidade sexual com maior tamanho corporal que os machos. O dimorfismo sexual não foi significativo para o tamanho da cabeça, mas os machos possuem caudas relativamente mais longas que as fêmeas. A vitelogênese, a postura de ovos e a espermatogênese ocorrem durante todo o ano, e os machos não armazenam esperma no ducto deferente por longos períodos. A principal presa dessa espécie são lagartos; não há evidencias de variação ontogenética ou de diferenças relacionadas ao sexo na dieta dessa espécie.

Parasites and pathogens lag behind their host during periods of host range advance.

The process of rapid range expansion (as seen in many invasive species, and in taxa responding to climate change) may substantially disrupt host-parasite dynamics. Parasites and pathogens can have strong regulatory effects on their host population and, in doing so, exert selection pressure on host life history. We construct a simple individual-based model of host-parasite dynamics during range expansion. This model shows that the parasites and pathogens of a range-expanding host are likely to be absent from the host's invasion front, because stochastic events (serial founder events) in low-density frontal populations result in local extinctions or transmission failure of the parasite/pathogen and, hence, a preponderance of uninfected hosts in the invasion vanguard. This pattern is true for both density-dependent and density-independent transmission rates, although it is exacerbated in the case of density-dependent transmission because, in this case, transmission rates also decline on the front. Data from field surveys on the prevalence of lungworms (Rhabdias pseudosphaerocephala) in invasive cane toads (Bufo marinus) support these predictions, in showing that toads in newly invaded areas of tropical Australia lack the parasite, which only arrives 1-3 years after the toads themselves. The resultant "honeymoon phase" immediately post-invasion, when individuals in the invasion-front population are virtually pathogen-free, may lead to altered host population dynamics on the invasion front, causing, for example, high densities in invasion-front populations, followed by a decline in numbers as parasites and pathogens arrive and begin to reduce host viability. The honeymoon phase may ultimately impact the evolution of life-history investment strategies in both host and parasite on the invasion vanguard, as hosts are released from immune challenges and parasites continuously expand into a favorable and unoccupied niche.

Estimating survival rates of uncatchable animals: the myth of high juvenile mortality in reptiles.

Survival rates of juvenile reptiles are critical population parameters but are difficult to obtain through mark-recapture programs because these small, secretive animals are rarely caught. This scarcity has encouraged speculation that survival rates of juveniles are very low, and we test this prediction by estimating juvenile survival rates indirectly. A simple mathematical model calculates the annual juvenile survival rate needed to maintain a stable population size, using published data on adult survival rates, reproductive output, and ages at maturity in 109 reptile populations encompassing 57 species. Counter to prediction, estimated juvenile survival rates were relatively high (on average, only about 13% less than those of conspecific adults) and highly correlated with adult survival rates. Overall, survival rates during both juvenile and adult life were higher in turtles than in snakes, and higher in snakes than in lizards. As predicted from life history theory, rates of juvenile survival were higher in species that produce large offspring, and higher in viviparous squamates than in oviparous species. Our analyses challenge the widely held belief that juvenile reptiles have low rates of annual survival and suggest instead that sampling problems and the elusive biology of juvenile reptiles have misled researchers in this respect.

Life-history adaptations to arboreality in snakes.

If selective forces on locomotor ability and reproductive biology differ among habitats, we expect to see relationships between habitat, morphology, and life-history traits. Comparative (phylogenetically based) analysis of data from 12 pythonid and 12 boid snake species reveals multiple evolutionary shifts in habitat use, notably in the evolution of arboreal habits. Compared to terrestrial and aquatic taxa of the same overall body size, arboreal species have narrower and more laterally compressed bodies and relatively longer tails. Offspring sizes are not affected by arboreality, but presumably reflecting space constraints within their narrow bodies, arboreal species (1) produce smaller clutch sizes relative to maternal body length and (2) have left and right ovaries that overlap little if at all along the length of the body (i.e., the right ovary is positioned anterior to the left ovary) whereas in terrestrial snakes the two ovaries overlap along much of their length. This modification of ovarian morphology in arboreal snakes presumably reduces the degree of bodily distension during vitellogenesis and pregnancy, thus enhancing climbing ability and camouflage among the branches.