Improving coral cover using an integrated pest management framework.

Integrated pest management (IPM) leverages our understanding of ecological interactions to mitigate the impact of pest species on economically and/or ecologically important assets. It has primarily been applied in terrestrial settings (e.g., agriculture), but has rarely been attempted for marine ecosystems. The crown-of-thorns starfish (CoTS), Acanthaster spp., is a voracious coral predator throughout the Indo-Pacific where it undergoes large population increases (irruptions), termed outbreaks. During outbreaks CoTS act as a pest species and can result in substantial coral loss. Contemporary management of CoTS on the Great Barrier Reef (GBR) adopts facets of the IPM paradigm to manage these outbreaks through strategic use of direct manual control (culling) of individuals in response to ecologically based target thresholds. There has, however, been limited quantitative analysis of how to optimize the implementation of such thresholds. Here we use a multispecies modeling approach to assess the performance of alternative CoTS management scenarios for improving coral cover trajectories. The scenarios examined varied in terms of their ecological threshold target, the sensitivity of the threshold, and the level of management resourcing. Our approach illustrates how to quantify multidimensional trade-offs in resourcing constraints, concurrent CoTS and coral population dynamics, the stringency of target thresholds, and the geographical scale of management outcomes (number of sites). We found strategies with low target density thresholds for CoTS (≤0.03 CoTS min-1 ) could act as "Effort Sinks" and limit the number of sites that could be effectively controlled, particularly under CoTS population outbreaks. This was because a handful of sites took longer to control, which meant other sites were not controlled. Higher density thresholds (e.g., 0.04-0.08 CoTS min-1 ), tuned to levels of coral cover, diluted resources among sites but were more robust to resourcing constraints and pest population dynamics. Our study highlights trade-off decisions when using an IPM framework and informs the implementation of threshold-based strategies on the GBR.

Dispersal and the design of effective management strategies for plant invasions: matching scales for success.

Dispersal of propagules makes invasions a fundamentally spatial phenomenon, and to be effective, management actions to control or eradicate invasive species must take this spatial structure into account. While there is a vibrant literature linking detailed dispersal measurements to the rate of invasive spread, and a separate literature focused on incorporating management into invasive models in order to improve the control of weeds, there are relatively fewer manuscripts incorporating state-of-the-art dispersal modeling and management modeling together to provide on-ground recommendations for structuring effective management. In this paper, we perform a generalized analysis of a spatially explicit, individual-based simulation model of invasion management with empirically determined dispersal processes, illustrated with the example of Miconia calvescens in the Australian Wet Tropics rain forest, to explore how matching the spatial scale of management to the spatial scale of the dispersal processes underpinning invasion influences the success of management. We find that management strategies designed to maximize the number of weeds removed from the management region, either in the first year of management or over longer periods, provide a poor estimate of the spatial scale of management that maximizes the probability of eradication. We show that achieving a goal of certainty of eradication requires exceeding a minimal spatial scale of management and total management resourcing. We generalize these results to examine how the spatial scale of dispersal drives the spatial scale of effective management strategies. These results show that to be effective, management of dispersal-driven invasions must occur at spatial scales determined by the scale of dispersal processes, and resourced accordingly. It illustrates how those scales might be calculated for a specific case for which detailed dispersal data are available and generalizes the result to highlight how dispersal scale drives the scale of effective management. The results highlight the importance of understanding the ecological drivers of invasion to structure effective management.

Implications of past and present genetic connectivity for management of the saltwater crocodile (Crocodylus porosus).

Effective management of protected species requires information on appropriate evolutionary and geographic population boundaries and knowledge of how the physical environment and life-history traits combine to shape the population structure and connectivity. Saltwater crocodiles (Crocodylus porosus) are the largest and most widely distributed of living crocodilians, extending from Sri Lanka to Southeast Asia and down to northern Australia. Given the long-distance movement capabilities reported for C. porosus, management units are hypothesised to be highly connected by migration. However, the magnitude, scale, and consistency of connection across managed populations are not fully understood. Here we used an efficient genotyping method that combines DArTseq and sequence capture to survey ≈ 3000 high-quality genome-wide single nucleotide polymorphisms from 1176 C. porosus sampled across nearly the entire range of the species in Queensland, Australia. We investigated historical and present-day connectivity patterns using fixation and diversity indices coupled with clustering methods and the spatial distribution of kin pairs. We inferred kinship using forward simulation coupled with a kinship estimation method that is robust to unspecified population structure. The results demonstrated that the C. porosus population has substantial genetic structure with six broad populations correlated with geographical location. The rate of gene flow was highly correlated with spatial distance, with greater differentiation along the east coast compared to the west. Kinship analyses revealed evidence of reproductive philopatry and limited dispersal, with approximately 90% of reported first and second-degree relatives showing a pairwise distance of <50 km between sampling locations. Given the limited dispersal, lack of suitable habitat, low densities of crocodiles and the high proportion of immature animals in the population, future management and conservation interventions should be considered at regional and state-wide scales.

Close-kin mark-recapture informs critically endangered terrestrial mammal status.

Reliable information on population size is fundamental to the management of threatened species. For wild species, mark-recapture methods are a cornerstone of abundance estimation. Here, we show the first application of the close-kin mark-recapture (CKMR) method to a terrestrial species of high conservation value; the Christmas Island flying-fox (CIFF). The CIFF is the island's last remaining native terrestrial mammal and was recently listed as critically endangered. CKMR is a powerful tool for estimating the demographic parameters central to CIFF management and circumvents the complications arising from the species' cryptic nature, mobility, and difficult-to-survey habitat. To this end, we used genetic data from 450 CIFFs captured between 2015 and 2019 to detect kin pairs. We implemented a novel CKMR model that estimates sex-specific abundance, trend, and mortality and accommodates observations from the kin-pair distribution of male reproductive skew and mate persistence. CKMR estimated CIFF total adult female abundance to be approximately 2050 individuals (95% CI (950, 4300)). We showed that on average only 23% of the adult male population contributed to annual reproduction and strong evidence for between-year mate fidelity, an observation not previously quantified for a Pteropus species in the wild. Critically, our population estimates provide the most robust understanding of the status of this critically endangered population, informing immediate and future conservation initiatives.

Assessment of monitoring power for highly mobile vertebrates.

Monitoring of population trends is a critical component of conservation management, and development of practical methods remains a priority, particularly for species that challenge more standard approaches. We used field-parameterized simulation models to examine the effects of different errors on monitoring power and compared alternative methods used with two species of threatened pteropodids (flying-foxes), Pteropus conspicillatus and P. poliocephalus, whose mobility violates assumptions of closure on short and long timescales. The influence of three errors on time to 80% statistical power was assessed using a Monte Carlo approach. The errors were: (1) failure to count all animals at a roost, (2) errors associated with enumeration, and (3) variability in the proportion of the population counted due to the movement of individuals between roosts. Even with perfect accuracy and precision for these errors only marginal improvements in power accrued (-1%), with one exception. Improving certainty in the proportion of the population being counted reduced time to detection of a decline by over 6 yr (43%) for fly-out counts and almost 10 yr (71%) for walk-through counts. This error derives from the movement of animals between known and unknown roost sites, violating assumptions of population closure, and because it applies to the entire population, it dominates all other sources of error. Similar errors will accrue in monitoring of a wide variety of highly mobile species and will also result from population redistribution under climate change. The greatest improvements in monitoring performance of highly mobile species accrue through an improved understanding of the proportion of the population being counted, and consequently monitoring of such species must be done at the scale of the species or population range, not at the local level.

Body-size dependent foraging strategies in the Christmas Island flying-fox: implications for seed and pollen dispersal within a threatened island ecosystem.

BACKGROUND: Animals are important vectors for the dispersal of a wide variety of plant species, and thus play a key role in maintaining the health and biodiversity of natural ecosystems. On oceanic islands, flying-foxes are often the only seed dispersers or pollinators. However, many flying-fox populations are currently in decline, particularly those of insular species, and this has consequences for the ecological services they provide. Knowledge of the drivers and the scale of flying-fox movements is important in determining the ecological roles that flying-foxes play on islands. This information is also useful for understanding the potential long-term consequences for forest dynamics resulting from population declines or extinction, and so can aid in the development of evidence-based ecological management strategies. To these ends, we examined the foraging movements, floral resource use, and social interactions of the Critically Endangered Christmas Island flying-fox (Pteropus natalis). METHODS: Utilization distributions, using movement-based kernel estimates (MBKE) were generated to determine nightly foraging movements of GPS-tracked P. natalis (n = 24). Generalized linear models (GLMs), linear mixed-effect models (LMMs), and Generalized linear mixed-effects model (GLMMs) were constructed to explain how intrinsic factors (body mass, skeletal size, and sex) affected the extent of foraging movements. In addition, we identified pollen collected from facial and body swabs of P. natalis (n = 216) to determine foraging resource use. Direct observations (n = 272) of foraging P. natalis enabled us to assess the various behaviors used to defend foraging resources. RESULTS: Larger P. natalis individuals spent more time foraging and less time traveling between foraging patches, traveled shorter nightly distances, and had smaller overall foraging ranges than smaller conspecifics. Additionally, larger individuals visited a lower diversity of floral resources. CONCLUSIONS: Our findings suggest that smaller P. natalis individuals are the primary vectors of long-distance dispersal of pollen and digested seeds in this species, providing a vital mechanism for maintaining the flow of plant genetic diversity across Christmas Island. Overall, our study highlights the need for more holistic research approaches that incorporate population demographics when assessing a species' ecological services.

Land use, season, and parasitism predict metal concentrations in Australian flying fox fur.

Urban-living wildlife can be exposed to metal contaminants dispersed into the environment through industrial, residential, and agricultural applications. Metal exposure carries lethal and sublethal consequences for animals; in particular, heavy metals (e.g. arsenic, lead, mercury) can damage organs and act as carcinogens. Many bat species reside and forage in human-modified habitats and could be exposed to contaminants in air, water, and food. We quantified metal concentrations in fur samples from three flying fox species (Pteropus fruit bats) captured at eight sites in eastern Australia. For subsets of bats, we assessed ectoparasite burden, haemoparasite infection, and viral infection, and performed white blood cell differential counts. We examined relationships among metal concentrations, environmental predictors (season, land use surrounding capture site), and individual predictors (species, sex, age, body condition, parasitism, neutrophil:lymphocyte ratio). As expected, bats captured at sites with greater human impact had higher metal loads. At one site with seasonal sampling, bats had higher metal concentrations in winter than in summer, possibly owing to changes in food availability and foraging. Relationships between ectoparasites and metal concentrations were mixed, suggesting multiple causal mechanisms. There was no association between overall metal load and neutrophil:lymphocyte ratio, but mercury concentrations were positively correlated with this ratio, which is associated with stress in other vertebrate taxa. Comparison of our findings to those of previous flying fox studies revealed potentially harmful levels of several metals; in particular, endangered spectacled flying foxes (P. conspicillatus) exhibited high concentrations of cadmium and lead. Because some bats harbor pathogens transmissible to humans and animals, future research should explore interactions between metal exposure, immunity, and infection to assess consequences for bat and human health.

Large-scale interventions may delay decline of the Great Barrier Reef.

On the iconic Great Barrier Reef (GBR), the cumulative impacts of tropical cyclones, marine heatwaves and regular outbreaks of coral-eating crown-of-thorns starfish (CoTS) have severely depleted coral cover. Climate change will further exacerbate this situation over the coming decades unless effective interventions are implemented. Evaluating the efficacy of alternative interventions in a complex system experiencing major cumulative impacts can only be achieved through a systems modelling approach. We have evaluated combinations of interventions using a coral reef meta-community model. The model consisted of a dynamic network of 3753 reefs supporting communities of corals and CoTS connected through ocean larval dispersal, and exposed to changing regimes of tropical cyclones, flood plumes, marine heatwaves and ocean acidification. Interventions included reducing flood plume impacts, expanding control of CoTS populations, stabilizing coral rubble, managing solar radiation and introducing heat-tolerant coral strains. Without intervention, all climate scenarios resulted in precipitous declines in GBR coral cover over the next 50 years. The most effective strategies in delaying decline were combinations that protected coral from both predation (CoTS control) and thermal stress (solar radiation management) deployed at large scale. Successful implementation could expand opportunities for climate action, natural adaptation and socioeconomic adjustment by at least one to two decades.

Relative efficacy of three approaches to mitigate Crown-of-Thorns Starfish outbreaks on Australia's Great Barrier Reef.

Population outbreaks of Crown-of-Thorns Starfish (COTS; Acanthaster spp.) are a major contributor to loss of hard coral throughout the Indo-Pacific. On Australia's Great Barrier Reef (GBR), management interventions have evolved over four COTS outbreaks to include: (1) manual COTS control, (2) Marine Protected Area (MPA) zoning, and, (3) water quality improvement. Here we evaluate the contribution of these three approaches to managing population outbreaks of COTS to minimize coral loss. Strategic manual control at sites reduced COTS numbers, including larger, more fecund and damaging individuals. Sustained reduction in COTS densities and improvements in hard coral cover at a site were achieved through repeated control visits. MPAs influenced initial COTS densities but only marginally influenced final hard coral cover following COTS control. Water quality improvement programs have achieved only marginal reductions in river nutrient loads delivered to the GBR and the study region. This, a subsequent COTS outbreak, and declining coral cover across the region suggest their contributions are negligible. These findings support manual control as the most direct, and only effective, means of reducing COTS densities and improving hard coral cover currently available at a site. We provide recommendations for improving control program effectiveness with application to supporting reef resilience across the Indo-Pacific.

Author Correction: DNA-based identification of predators of the corallivorous Crown-of-Thorns Starfish (Acanthaster cf. solaris) from fish faeces and gut contents.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

DNA-based identification of predators of the corallivorous Crown-of-Thorns Starfish (Acanthaster cf. solaris) from fish faeces and gut contents.

The corallivorous Crown-of-Thorns Starfish (CoTS, Acanthaster spp.) has been linked with the widespread loss of scleractinian coral cover on Indo-Pacific reefs during periodic population outbreaks. Here, we re-examine CoTS consumption by coral reef fish species by using new DNA technologies to detect Pacific Crown-of-Thorns Starfish (Acanthaster cf. solaris) in fish faecal and gut content samples. CoTS DNA was detected in samples from 18 different coral reef fish species collected on reefs at various stages of CoTS outbreaks in the Great Barrier Reef Marine Park, nine of which had not been previously reported to feed on CoTS. A comprehensive set of negative and positive control samples confirmed that our collection, processing and analysis procedures were robust, although food web transfer of CoTS DNA cannot be ruled out for some fish species. Our results, combined with the (i) presence of CoTS spines in some samples, (ii) reported predation on CoTS gametes, larvae and settled individuals, and (iii) known diet information for fish species examined, strongly indicate that direct fish predation on CoTS may well be more common than is currently appreciated. We provide recommendations for specific management approaches to enhance predation on CoTS by coral reef fishes, and to support the mitigation of CoTS outbreaks and reverse declines in hard coral cover.

Molecular investigation of Hepatocystis parasites in the Australian flying fox Pteropus poliocephalus across its distribution range.

Phylogenetic inference of Hepatocystis, a haemosporidian parasite of diverse primate and bat hosts, revealed that the parasites from Australasian Pteropus bat species form a distinct clade to all other Hepatocystis parasites from Africa and Asia. Here, we investigate the phylogenetic placement of Hepatocystis in the Australian bat Pteropus poliocephalus for the first time and examine parasite morphology and prevalence from selected points across its range. Hepatocystis infections were detected in low prevalences in P. poliocephalus in contrast to high numbers in P. alecto and P. scapulatus. The prevalence in P. poliocephalus varied across its distribution range with 15% in the central biogeographic areas (central Queensland and New South Wales) and 1% in the southern-most edge (South Australia) of its range. Sequencing of five genes revealed high genetic similarity in Hepatocystis of P. poliocephalus independent of sampling location. Phylogenetic analysis placed these parasites with Hepatocystis from other Pteropus species from Australia and Asia. While numerous haplotypes were identified among sequences from the Pteropus hosts, no patterns of host specificity were recovered within the Pteropus-specific parasite group.

Using weather radar to monitor the number, timing and directions of flying-foxes emerging from their roosts.

Knowledge of species' population trends is crucial when planning for conservation and management; however, this information can be difficult to obtain for extremely mobile species such as flying-foxes (Pteropus spp.; Chiroptera, Pteropodidae). In mainland Australia, flying-foxes are of particular management concern due their involvement in human-wildlife conflict, and their role as vectors of zoonotic diseases; and two species, the grey-headed flying-fox (Pteropus poliocephalus) and the spectacled flying-fox (P. conspicillatus), are currently threatened with extinction. Here we demonstrate that archival weather radar data over a period of ten years can be used to monitor a large colony of grey-headed flying-foxes near Melbourne. We show that radar estimates of colony size closely match those derived from traditional counting methods. Moreover, we show that radar data can be used to determine the timing and departure direction of flying-foxes emerging from the roost. Finally, we show that radar observations of flying-foxes can be used to identify signals of important ecological events, such as mass flowering and extreme heat events, and can inform human activities, e.g. the safe operation of airports and windfarms. As such, radar represents an extremely promising tool for the conservation and management of vulnerable flying-fox populations and for managing human interactions with these ecologically-important mammals.

A state-space modelling approach to wildlife monitoring with application to flying-fox abundance.

Monitoring flying-foxes is challenging as their extreme mobility produces highly dynamic population processes, considerable logistic difficulty, and variability in estimated population size. We report on methods for inferring population trend for the population of the spectacled flying-fox (Pteropus conspicillatus) in Australia. Monthly monitoring is conducted at all known roost sites across the species' range in the Wet Tropics Region. The proportion of animals in camps varies seasonally and stochastic environmental events appear to be influential. We develop a state-space model that incorporates these processes and enables inference on total population trends and uses early warning analysis to identify the causes of population dynamics. The model suggests that population growth rate is stable in the absence of cyclones, however, cyclones appear to impact on both survival and reproduction. The population recovered after two cyclones but declined after a third. The modelling estimates a population decline over 15 years of c. 75% (mean r = - 0.12yr-1 and belief of negative trend is c. 83%) suggesting that conservation action is warranted. Our work shows that a state-space modelling approach is a significant improvement on inference from raw counts from surveys and demonstrates that this approach is a workable alternative to other methods.

Slow growth and delayed maturation in a Critically Endangered insular flying fox (Pteropus natalis).

Flying foxes (family Pteropodidae) have distinct life histories given their size, characterized by longevity, low reproductive output, and long gestation. However, they tend to decouple the age at which sexual maturity is reached from the age at which they reach adult dimensions. We examined growth, maturation, and reproduction in the Critically Endangered Christmas Island flying fox (Pteropus natalis) to determine the timing of sex-specific life cycle events and patterns of growth. We estimated that juvenile growth in forearm length and body mass increased at a mean rate of 0.029 ± 0.005 mm/day and 0.33 ± 0.07 g/day for both males and females alike. Using these growth rates, we determined that the birth of pups occurs between December and March, with young becoming volant between June and August. The age at maturation for P. natalis is one of the oldest among all bat species. Juvenile males began to mature 15 months after birth and reached maturity 27 months after birth. Females reached maturity 24 months after birth at a significantly smaller body mass (3.6%) and forearm length (1.4%) than males. Significant sexual dimorphism and bimaturation was observed, with juvenile males being 1.5% and adult males being 1.9% larger on average than females for skeletal dimensions only. Growth and maturation are even slower in P. natalis than in the few other Pteropus species studied to date. The slow growth and delayed maturation of P. natalis imply slower potential population growth rates, further complicating the recovery of this Critically Endangered single-island endemic.

Environmental drivers of spatiotemporal foraging intensity in fruit bats and implications for Hendra virus ecology.

In the Australian subtropics, flying-foxes (family Pteropididae) play a fundamental ecological role as forest pollinators. Flying-foxes are also reservoirs of the fatal zoonosis, Hendra virus. Understanding flying fox foraging ecology, particularly in agricultural areas during winter, is critical to determine their role in transmitting Hendra virus to horses and humans. We developed a spatiotemporal model of flying-fox foraging intensity based on foraging patterns of 37 grey-headed flying-foxes (Pteropus poliocephalus) using GPS tracking devices and boosted regression trees. We validated the model with independent population counts and summarized temporal patterns in terms of spatial resource concentration. We found that spatial resource concentration was highest in late-summer and lowest in winter, with lowest values in winter 2011, the same year an unprecedented cluster of spillover events occurred in Queensland and New South Wales. Spatial resource concentration was positively correlated with El Niño Southern Oscillation at 3-8 month time lags. Based on shared foraging traits with the primary reservoir of Hendra virus (Pteropus alecto), we used our results to develop hypotheses on how regional climatic history, eucalypt phenology, and foraging behaviour may contribute to the predominance of winter spillovers, and how these phenomena connote foraging habitat conservation as a public health intervention.

Body size and substrate type modulate movement by the western Pacific crown-of-thorns starfish, Acanthaster solaris.

The movement capacity of the crown-of-thorns starfishes (Acanthaster spp.) is a primary determinant of both their distribution and impact on coral assemblages. We quantified individual movement rates for the Pacific crown-of-thorns starfish (Acanthaster solaris) ranging in size from 75-480 mm total diameter, across three different substrates (sand, flat consolidated pavement, and coral rubble) on the northern Great Barrier Reef. The mean (±SE) rate of movement for smaller (<150 mm total diameter) A. solaris was 23.99 ± 1.02 cm/ min and 33.41 ± 1.49 cm/ min for individuals >350 mm total diameter. Mean (±SE) rates of movement varied with substrate type, being much higher on sand (36.53 ± 1.31 cm/ min) compared to consolidated pavement (28.04 ± 1.15 cm/ min) and slowest across coral rubble (17.25 ± 0.63 cm/ min). If average rates of movement measured here can be sustained, in combination with strong directionality, displacement distances of adult A. solaris could range from 250-520 m/ day, depending on the prevailing substrate. Sustained movement of A. solaris is, however, likely to be highly constrained by habitat heterogeneity, energetic constraints, resource availability, and diurnal patterns of activity, thereby limiting their capacity to move between reefs or habitats.

Global transcriptomic profiling in barramundi (Lates calcarifer) from rivers impacted by differing agricultural land uses.

Most catchments discharging into the Great Barrier Reef lagoon have elevated loads of suspended sediment, nutrients, and pesticides, including photosystem II inhibiting herbicides, associated with upstream agricultural land use. To investigate potential impacts of declining water quality on fish physiology, RNA sequencing (RNASeq) was used to characterize and compare the hepatic transcriptomes of barramundi (Lates calcarifer) captured from 2 of these tropical river catchments in Queensland, Australia. The Daintree and Tully Rivers differ in upstream land uses, as well as sediment, nutrient, and pesticide loads, with the area of agricultural land use and contaminant loads lower in the Daintree. In fish collected from the Tully River, transcripts involved in fatty acid metabolism, amino acid metabolism, and citrate cycling were also more abundant, suggesting elevated circulating cortisol concentrations, whereas transcripts involved in immune responses were less abundant. Fish from the Tully also had an increased abundance of transcripts associated with xenobiotic metabolism. Previous laboratory-based studies observed similar patterns in fish and amphibians exposed to the agricultural herbicide atrazine. If these transcriptomic patterns are manifested at the whole organism level, the differences in water quality between the 2 rivers may alter fish growth and fitness. Environ Toxicol Chem 2017;36:103-112. © 2016 SETAC.

Animal visual systems and the evolution of color patterns: sensory processing illuminates signal evolution.

Animal color pattern phenotypes evolve rapidly. What influences their evolution? Because color patterns are used in communication, selection for signal efficacy, relative to the intended receiver's visual system, may explain and predict the direction of evolution. We investigated this in bowerbirds, whose color patterns consist of plumage, bower structure, and ornaments and whose visual displays are presented under predictable visual conditions. We used data on avian vision, environmental conditions, color pattern properties, and an estimate of the bowerbird phylogeny to test hypotheses about evolutionary effects of visual processing. Different components of the color pattern evolve differently. Plumage sexual dimorphism increased and then decreased, while overall (plumage plus bower) visual contrast increased. The use of bowers allows relative crypsis of the bird but increased efficacy of the signal as a whole. Ornaments do not elaborate existing plumage features but instead are innovations (new color schemes) that increase signal efficacy. Isolation between species could be facilitated by plumage but not ornaments, because we observed character displacement only in plumage. Bowerbird color pattern evolution is at least partially predictable from the function of the visual system and from knowledge of different functions of different components of the color patterns. This provides clues to how more constrained visual signaling systems may evolve.