Population genetics of the frog-killing fungus Batrachochytrium dendrobatidis

Global amphibian decline by chytridiomycosis is a major environmental disaster that has been attributed to either recent fungal spread or environmental change that promotes disease. Here, we present a population genetic comparison of Batrachochytrium dendrobatidis isolates from an intensively studied region of frog decline, the Sierra Nevada of California. In support of a novel pathogen, we find low diversity, no amphibian-host specificity, little correlation between fungal genotype and geography, local frog extirpation by a single fungal genotype, and evidence of human-assisted fungus migration. In support of endemism, at a local scale, we find some diverse, recombining populations. Therefore neither epidemic spread nor endemism alone explains this particular amphibian decline. Recombination raises the possibility of resistant sporangia and a mechanism for rapid spread as well as persistence that could greatly complicate global control of the pathogen.

Recovery of the red-finned blue-eye: An endangered fish from springs of the Great Artesian Basin

The red-finned blue-eye (Scaturiginichthys vermeilipinnis) is endemic to a single complex of springs emanating from the Great Artesian Basin, Australia. The species has been recorded as naturally occurring in eight separate very shallow (generally <20 mm) springs, with a combined wetland area of ~0.3 ha. Since its discovery in 1990, five red-finned blue-eye (RFBE) populations have been lost and subsequent colonisation has occurred in two spring wetlands. Current population size is estimated at <3000 individuals. Artesian bores have reduced aquifer pressure, standing water levels and spring-flows in the district. There is evidence of spatial separation within the spring pools where RFBE and the introduced fish gambusia (Gambusia holbrooki) co-occur, although both species are forced together when seasonal extremes affect spring size and water temperature. Gambusia was present in four of the five springs where RFBE populations have been lost. Four out of the five remaining subpopulations of RFBE are Gambusia free. Circumstantial evidence suggests that gambusia is a major threat to red-finned blue-eyes. The impact of Gambusia is probably exacerbated by domestic stock (cattle and sheep), feral goats and pigs that utilise the springs and can negatively affect water quality and flow patterns. Three attempts to translocate RFBE to apparently suitable springs elsewhere within the complex have failed. Opportunities to mitigate threats are discussed, along with directions for future research to improve management of this extremely threatened fish and habitat.

Rapid Global Expansion of the Fungal Disease Chytridiomycosis into Declining and Healthy Amphibian Populations.

The fungal disease chytridiomycosis, caused by Batrachochytrium dendrobatidis, is enigmatic because it occurs globally in both declining and apparently healthy (non-declining) amphibian populations. This distribution has fueled debate concerning whether, in sites where it has recently been found, the pathogen was introduced or is endemic. In this study, we addressed the molecular population genetics of a global collection of fungal strains from both declining and healthy amphibian populations using DNA sequence variation from 17 nuclear loci and a large fragment from the mitochondrial genome. We found a low rate of DNA polymorphism, with only two sequence alleles detected at each locus, but a high diversity of diploid genotypes. Half of the loci displayed an excess of heterozygous genotypes, consistent with a primarily clonal mode of reproduction. Despite the absence of obvious sex, genotypic diversity was high (44 unique genotypes out of 59 strains). We provide evidence that the observed genotypic variation can be generated by loss of heterozygosity through mitotic recombination. One strain isolated from a bullfrog possessed as much allelic diversity as the entire global sample, suggesting the current epidemic can be traced back to the outbreak of a single clonal lineage. These data are consistent with the current chytridiomycosis epidemic resulting from a novel pathogen undergoing a rapid and recent range expansion. The widespread occurrence of the same lineage in both healthy and declining populations suggests that the outcome of the disease is contingent on environmental factors and host resistance.

Inter-seasonal population dynamics and pest status of Bemisia tabaci (Gennadius) biotype B in an Australian cropping system

Bemisia tabaci, biotype B, commonly known as the silverleaf whitefly (SLW) is an alien species that invaded Australia in the mid-90s. This paper reports on the invasion ecology of SLW and the factors that are likely to have contributed to the first outbreak of this major pest in an Australian cotton cropping system, population dynamics of SLW within whitefly-susceptible crop (cotton and cucurbit) and non-crop vegetation (sowthistle, Sonchus spp.) components of the cropping system were investigated over four consecutive growing seasons (September-June) 2001/02-2004/05 in the Emerald Irrigation Area (EIA) of Queensland, Australia. Based on fixed geo-referenced sampling sites, variation in spatial and temporal abundance of SLW within each system component was quantified to provide baseline data for the development of ecologically sustainable pest management strategies. Parasitism of large (3rd and 4th instars) SLW nymphs by native aphelinid wasps was quantified to determine the potential for natural control of SLW populations. Following the initial outbreak in 2001/02, SLW abundance declined and stabilised over the next three seasons. The population dynamics of SLW is characterised by inter-seasonal population cycling between the non-crop (weed) and cotton components of the EIA cropping system. Cotton was the largest sink for and source of SLW during the study period. Over-wintering populations dispersed from weed host plant sources to cotton in spring followed by a reverse dispersal in late summer and autumn to broad-leaved crops and weeds. A basic spatial source-sink analysis showed that SLW adult and nymph densities were higher in cotton fields that were closer to over-wintering weed sources throughout spring than in fields that were further away. Cucurbit fields were not significant sources of SLW and did not appear to contribute significantly to the regional population dynamics of the pest. Substantial parasitism of nymphal stages throughout the study period indicates that native parasitoid species and other natural enemies are important sources of SLW mortality in Australian cotton production systems. Weather conditions and use of broad-spectrum insecticides for pest control are implicated in the initial outbreak and on-going pest status of SLW in the region.

Population dynamics of the European rabbit (Oryctolagus cuniculus) in north eastern Australia: simulated responses to control

Wild European rabbits are a serious problem to agriculture in Australia, with an estimated annual cost of A$ 113 million. Biological control agents (myxomatosis and rabbit haemorrhagic disease virus) have caused large and sustained declines in rabbit populations throughout Australia. A simulation model incorporates these diseases as well as warren destruction as methods of controlling rabbit populations in Queensland, north eastern Australia. These diseases reduced populations by 90-99% and the combination of these and warren destruction led to 100% control in simulations at six sites across southern Queensland. Increasing monthly pasture growth by 15% had little effect on simulated populations whereas a 15% decrease reduced populations by 0-50%. An increase in temperature of 2.5 °C would lead to a 15-60% decrease in populations. These effects suggest that climate change will lead to a decrease in the population of rabbits in Queensland and a retraction in the northern limit of their distribution in Australia.

Stochastic demography and population dynamics in the red kangaroo Macropus rufus

1. Many organisms inhabit strongly fluctuating environments but their demography and population dynamics are often analysed using deterministic models and elasticity analysis, where elasticity is defined as the proportional change in population growth rate caused by a proportional change in a vital rate. Deterministic analyses may not necessarily be informative because large variation in a vital rate with a small deterministic elasticity may affect the population growth rate more than a small change in a less variable vital rate having high deterministic elasticity. 2. We analyse a stochastic environment model of the red kangaroo (Macropus rufus), a species inhabiting an environment characterized by unpredictable and highly variable rainfall, and calculate the elasticity of the stochastic growth rate with respect to the mean and variability in vital rates. 3. Juvenile survival is the most variable vital rate but a proportional change in the mean adult survival rate has a much stronger effect on the stochastic growth rate. 4. Even if changes in average rainfall have a larger impact on population growth rate, increased variability in rainfall may still be important also in long-lived species. The elasticity with respect to the standard deviation of rainfall is comparable to the mean elasticities of all vital rates but the survival in age class 3 because increased variation in rainfall affects both the mean and variability of vital rates. 5. Red kangaroos are harvested and, under the current rainfall pattern, an annual harvest fraction of c. 20% would yield a stochastic growth rate about unity. However, if average rainfall drops by more than c. 10%, any level of harvesting may be unsustainable, emphasizing the need for integrating climate change predictions in population management and increase our understanding of how environmental stochasticity translates into population growth rate.

Demography of feral camels in central Australia and its relevance to population control

Since their release over 100 years ago, camels have spread across central Australia and increased in number. Increasingly, they are being seen as a pest, with observed impacts from overgrazing and damage to infrastructure such as fences. Irregular aerial surveys since 1983 and an interview-based survey in 1966 suggest that camels have been increasing at close to their maximum rate. A comparison of three models of population growth fitted to these, albeit limited, data suggests that the Northern Territory population has indeed been growing at an annual exponential rate of r = 0.074, or 8% per year, with little evidence of a density-dependent brake. A stage-structured model using life history data from a central Australian camel population suggests that this rate approximates the theoretical maximum. Elasticity analysis indicates that adult survival is by far the biggest influence on rate of increase and that a 9% reduction in survival from 96% is needed to stop the population growing. In contrast, at least 70% of mature females need to be sterilised to have a similar effect. In a benign environment, a population of large mammals such as camels is expected to grow exponentially until close to carrying capacity. This will frustrate control programs, because an ever-increasing number of animals will need to be removed for zero growth the longer that culling or harvesting effort is delayed. A population projection for 2008 suggests ~10 500 animals need to be harvested across the Northern Territory. Current harvests are well short of this. The ability of commercial harvesting to control camel populations in central Australia will depend on the value of animals, access to animals and the presence of alternative species to harvest when camels are at low density.

Population structure of South African and Australian Pyrenophora teres isolates.

There are two recognized forms of the disease net blotch of barley: the net form caused by Pyrenophora teres f. teres (PTT) and the spot form caused by P. teres f. maculata (PTM). In this study, amplified fragment length polymorphism analysis was used to investigate the genetic diversity and population structure of 60 PTT and 64 PTM isolates collected across Australia (66 isolates) and in the south-western Cape of South Africa (58 isolates). For comparison, P. tritici-repentis, Exserohilum rostratum and Bipolaris sorokiniana samples were also included in the analyses. Both distance-and model-based cluster analyses separated the PTT and PTM isolates into two strongly divergent genetic groups. Significant variation was observed both among the South African and Australian populations of PTT and PTM and among sampling locations for the PTT samples. Results suggest that sexual reproduction between the two forms is unlikely and that reproduction within the PTT and PTM groups occurs mainly asexually.

Impacts of grazing management options on pasture and animal productivity in a Heteropogon contortus (black speargrass) pasture in central Queensland. 2. Population dynamics of Heteropogon contortus and Stylosanthes scabra cv. Seca.

The dynamics of Heteropogon contortus and Stylosanthes scabra cv. Seca populations were studied in a subset of treatments in an extensive grazing study conducted in central Queensland between 1988 and 2001. These treatments were 4 stocking rates in native pasture and 2 of these stocking rates in legume oversown and supplement/spring burning treatments. For the 1999-2000 summer, population data for H. contortus in 5 of these native pasture and supplement/burning treatments were compared with those for an additional burnt treatment. Seasonal rainfall throughout this study was below the long-term mean and mean annual pasture utilisation ranged from 24 to 61%. Increasing stocking rate from 5 to 2 ha/steer in native pasture reduced H. contortus plant density. Increasing stocking rate reduced seedling recruitment as a result of its effect on soil seedbanks. Seedling recruitment was the major determinant of change in plant density, although some individual H. contortus plants did survive throughout the study. Burning in spring 1999, particularly at light stocking rate, promoted seedling recruitment above that in both unburnt native and legume oversown pasture and resulted in increased H. contortus plant density. In the legume oversown treatments, S. scabra cv. Seca density increased rapidly from 15 plants/m2 in 1988 to 140 plants/m2 in 2001 following a lag phase between 1988 and 1993. This increased S. scabra density was associated with an eventual decline in H. contortus plant density through reduced seedling recruitment. It was concluded that H. contortus population density is sustainable at stocking rates of 4 and 5 ha/steer (30% pasture utilisation) and that spring burning at light stocking rate can promote H. contortus populations. Increasing densities of S. scabra need to be managed to prevent its dominance.

Grey Mackerel (Scomberomorus semifasciatus) microsatellite genotypes (nine loci) representing twelve regions along Australia's northern coastline from the eastern coast of Queensland to the western coast of Western Australia.

Scomberomorus semifasciatus is an Australian endemic found in tropical, coastal waters from eastern to western Australia. Commercial and recreational exploitation is common and regulated by state-based authorities. This study used mitochondrial DNA sequence and microsatellite markers to elucidate the population structure of Scomberomorus semifasciatus collected from twelve, equidistant sampling locations. Samples (n=544) were genotyped with nine microsatellite loci, and 353 were sequenced for d-loop (384 bp) and ATP (800bp) mitochondrial DNA gene regions. Combined interpretation of microsatellite and mtDNA data identified four genetic stocks of S. semifasciatus: Western Australia, northwest coast of the Northern Territory, Gulf of Carpentaria and the east coast of Queensland. Connectivity among stocks across northern Australia from the Northern Territory to the east coast of Queensland was high, but in contrast, there was a clear genetic break between populations in Western Australia compared to the rest of northern Australia. This indicates a restriction to gene flow possibly associated with suboptimal habitat along the Kimberley coast (northwestern Australia). The appropriate scale of management for this species corresponds to the jurisdictions of the three Australian states, except that the Gulf of Carpentaria stock should be co-managed by authorities in Queensland and Northern Territory.

Population structure, effective population size and adverse effects of stocking in the endangered Australian eastern freshwater cod Maccullochella ikei

Microsatellite markers were used to examine spatio-temporal genetic variation in the endangered eastern freshwater cod Maccullochella ikei in the Clarence River system, eastern Australia. High levels of population structure were detected. A model-based clustering analysis of multilocus genotypes identified four populations that were highly differentiated by F-statistics (FST = 0· 09 − 0· 49; P < 0· 05), suggesting fragmentation and restricted dispersal particularly among upstream sites. Hatchery breeding programmes were used to re-establish locally extirpated populations and to supplement remnant populations. Bayesian and frequency-based analyses of hatchery fingerling samples provided evidence for population admixture in the hatchery, with the majority of parental stock sourced from distinct upstream sites. Comparison between historical and contemporary wild-caught samples showed a significant loss of heterozygosity (21%) and allelic richness (24%) in the Mann and Nymboida Rivers since the commencement of stocking. Fragmentation may have been a causative factor; however, temporal shifts in allele frequencies suggest swamping with hatchery-produced M. ikei has contributed to the genetic decline in the largest wild population. This study demonstrates the importance of using information on genetic variation and population structure in the management of breeding and stocking programmes, particularly for threatened species.

Negligible evidence for regional genetic population structure for two shark species Rhizoprionodon acutus (Rüppell, 1837) and Sphyrna lewini (Griffith & Smith, 1834) with contrasting biology

Biodiversity of sharks in the tropical Indo-Pacific is high, but species-specific information to assist sustainable resource exploitation is scarce. The null hypothesis of population genetic homogeneity was tested for scalloped hammerhead shark (Sphyrna lewini, n = 237) and the milk shark (Rhizoprionodon acutus, n = 207) from northern and eastern Australia, using nuclear (S. lewini, eight microsatellite loci; R. acutus, six loci) and mitochondrial gene markers (873 base pairs of NADH dehydrogenase subunit 4). We were unable to reject genetic homogeneity for S. lewini, which was as expected based on previous studies of this species. Less expected were similar results for R. acutus, which is more benthic and less vagile than S. lewini. These features are probably driving the genetic break found between Australian and central Indonesian R. acutus (F-statistics; mtDNA, 0.751–0.903, respectively; microsatellite loci, 0.038–0.047 respectively). Our results support the spatially homogeneous monitoring and management plan for shark species in Queensland, Australia.

Evidence for extensive population structure in the white-spotted eagle ray within the Indo-Pacific inferred from mitochondrial gene sequences

The white-spotted eagle ray Aetobatus narinari is a species complex that occurs circumglobally throughout warm-temperate waters. Aetobatus narinari is semi-pelagic and large (up to 300 cm disc width), suggesting high dispersal capabilities and gene flow on a wide spatial scale. Sequence data from two mitochondrial genes, cytochrome b (cytb) and NADH dehydrogenase subunit 4 (ND4), were used to determine the genetic variability within and among 18 sampling locations in the central Indo-Pacific biogeographical region. Populations in the Indo-Pacific were highly genetically structured with c. 70% of the total genetic variation found among three geographical regions (East China Sea, Southeast Asia and Australia). FST was 0.64 for cytb and 0.53 for ND4, with φST values being even larger, that is, 0.78 for cytb and 0.65 for ND4. This high-level genetic partitioning provides strong evidence against extensive gene flow in A. narinari. The degree of genetic population structuring in the Indo-Pacific was similar to that found on a global scale. Global FST was 0.63 for cytb and 0.57 for ND4, and global φST values were 0.94 for cytb and 0.82 for ND4. This suggests that the A. narinari complex may be more speciose than the two or three species proposed to date. Further sampling and genetic analyses are likely to uncover the ‘evolutionarily significant’ and ‘management’ units that are critical to determine the susceptibilities of individual populations to regional fishing pressures and to provide advice on management options. Network analyses showed a close genetic relationship between haplotypes from the central Indo-Pacific and South Africa, providing support for a proposed dispersal pathway from the possible centre of origin of the A. narinari species complex in the Indo-Pacific into the Atlantic Ocean.

Population genetic evidence for the east–west division of the narrow-barred Spanish mackerel (Scomberomorus commerson, Perciformes: Teleostei) along Wallace’s Line

Mitochondrial DNA D-loop (control) region (426-bp) was used to infer the genetic structure of Spanish mackerel (Scomberomorus commerson) from populations in Southeast Asia (Brunei, East and West Malaysia, Philippines, Thailand, Singapore, and China) and northern Australia (including western Timor). An east–west division along Wallace’s Line was strongly supported by a significant AMOVA, with 43% of the total sequence variation partitioned among groups of populations. Phylogenetic and network analyses supported two clades: clade A and clade B. Members of clade A were found in Southeast Asia and northern Australia, but not in locations to the west (Gulf of Thailand) or north (China). Clade B was found exclusively in Southeast Asia. Genetic division along Wallace’s Line suggests that co-management of S. commerson populations for future sustainability may not be necessary between Southeast Asian nations and Australia, however all countries should share the task of management of the species in Southeast Asia equally. More detailed genetic studies of S. commerson populations in the region are warranted.

The extent of population genetic subdivision differs among four co-distributed shark species in the Indo-Australian archipelago

Background: The territorial fishing zones of Australia and Indonesia are contiguous to the north of Australia in the Timor and Arafura Seas and in the Indian Ocean to the north of Christmas Island. The area surrounding the shared boundary consists of a variety of bio-diverse marine habitats including shallow continental shelf waters, oceanic trenches and numerous offshore islands. Both countries exploit a variety of fisheries species, including whaler (Carcharhinus spp.) and hammerhead sharks (Sphyrna spp.). Despite their differences in social and financial arrangements, the two countries are motivated to develop complementary co-management practices to achieve resource sustainability. An essential starting point is knowledge of the degree of population subdivision, and hence fisheries stock status, in exploited species. Results: Populations of four commercially harvested shark species (Carcharhinus obscurus, Carcharhinus sorrah, Prionace glauca, Sphyrna lewini) were sampled from northern Australia and central Indonesia. Neutral genetic markers (mitochondrial DNA control region sequence and allelic variation at co-dominant microsatellite loci) revealed genetic subdivision between Australian and Indonesian populations of C. sorrah. Further research is needed to address the possibility of genetic subdivision among C. obscurus populations. There was no evidence of genetic subdivision for P. glauca and S. lewini populations, but the sampling represented a relatively small part of their distributional range. For these species, more detailed analyses of population genetic structure is recommended in the future. Conclusion: Cooperative management between Australia and Indonesia is the best option at present for P. glauca and S. lewini, while C. sorrah and C. obscurus should be managed independently. On-going research on these and other exploited shark and ray species is strongly recommended. Biological and ecological similarity between species may not be a predictor of population genetic structure, so species-specific studies are recommended to provide new data to assist with sustainable fisheries management.