Helmeted Honeyeater Research Articles

Benefits of genetic rescue of a critically endangered subspecies from another subspecies outweigh risks: Results of captive breeding trials

Small, isolated populations risk extinction through inbreeding depression, chance loss of beneficial variation, and reduced adaptability to changing environments. Genetic rescue via gene flow from genetically diverse sources is the most effective way to improve fitness of such populations. However, when the only potential source of immigrants is a different subspecies that diverged long ago and occupies a different environment, genetic rescue may lead to reduced fitness of admixed offspring through outbreeding depression or maladaptation. Test cases are needed to evaluate how to manage such potentially risky rescues to deliver enhanced population fitness. The helmeted honeyeater Lichenostomus melanops cassidix is a critically endangered subspecies of the yellow-tufted honeyeater. The sole remaining natural wild population experiences strong inbreeding depression for lifetime reproductive fitness. Captive genetic rescue trials are underway using a neighbouring subspecies, gippslandicus, which diverged from cassidix thousands of years ago and differs in morphology, mobility and preferred habitat. We evaluated short-term reproductive fitness for captive cassidix-cassidix pairs, first- and second-generation intersubspecific crosses and backcrosses to cassidix, while accounting for breeding season, sex, age at breeding, and wild/captive origin of each bird. Most admixed pair-types more readily engaged in breeding, raised more nestlings per nest, and had less male-biased chick sex-ratios than did cassidix-cassidix pairs, with negligible evidence of outbreeding depression. Continuing monitoring of fitness after releases into the wild is recommended, to ensure local adaptation is retained. With potentially riskier rescue increasingly becoming the only option for many populations, our study provides an encouraging test case.

Can we save Australia’s endangered wildlife by increasing species recognition?

Australia’s species extinction rate is one of the highest in the world. Yet, there is limited evidence regarding people’s recognition of, and preferences and support for, Australian endangered wildlife. This paper presents survey responses from 223 Zoos Victoria visitors (response rate: 39.1 %) and 90 community members (Victoria, Australia). We examined people’s top 10 overall (global) and Australian favourite animals, and conducted an in-depth exploration of recognition of, and preferences and support for, seven Australian endangered species identified as being at risk of extinction within the next decade, including: the leadbeater’s possum (Gymnobelideus leadbeateri), eastern barred bandicoot (Perameles gunnii), helmeted honeyeater (Lichenostomus melanops cassidix), southern corroboree frog (Pseudophryne corroboree), Lord Howe Island (LHI) stick insect (Dryococelus australis), Tasmanian devil (Sarcophilus harrisii), and the orange-bellied parrot (Neophema chrysogaster). Results indicate that the only Australian animals to feature in the overall top 10 favourite list were the kangaroo (ranked 9th for both sample groups) and koala (ranked 6th and 10th for the community and zoo sample, respectively). The Tasmanian devil had the highest rate of recognition (>86 %), in comparison to the remaining six species (1.2–7.3 % across both samples). Endangered species were not prominent in the top favourite Australian species. Australian endangered species’ likeability ratings typically followed the pattern of mammals being most likeable (Tasmanian devil and leadbeater’s possum), followed by birds, frogs, and insects (helmeted honeyeater, southern corroboree frog, and LHI stick insect). Importantly, for most endangered native species featured (4/7 and 6/7; zoo and community, respectively), simply being able to recognise species significantly (p <.05) increased people’s willingness to support their conservation. Findings underscore several powerful opportunities for future conservation programs to contribute to Australian endangered species conservation by striving to increase public familiarity with Australian species most at risk of extinction.

Chromosome-length genome assembly and linkage map of a critically endangered Australian bird: the helmeted honeyeater.

BackgroundThe helmeted honeyeater (Lichenostomus melanops cassidix) is a Critically Endangered bird endemic to Victoria, Australia. To aid its conservation, the population is the subject of genetic rescue. To understand, monitor, and modulate the effects of genetic rescue on the helmeted honeyeater genome, a chromosome-length genome and a high-density linkage map are required.ResultsWe used a combination of Illumina, Oxford Nanopore, and Hi-C sequencing technologies to assemble a chromosome-length genome of the helmeted honeyeater, comprising 906 scaffolds, with length of 1.1 Gb and scaffold N50 of 63.8 Mb. Annotation comprised 57,181 gene models. Using a pedigree of 257 birds and 53,111 single-nucleotide polymorphisms, we obtained high-density linkage and recombination maps for 25 autosomes and Z chromosome. The total sex-averaged linkage map was 1,347 cM long, with the male map being 6.7% longer than the female map. Recombination maps revealed sexually dimorphic recombination rates (overall higher in males), with average recombination rate of 1.8 cM/Mb. Comparative analyses revealed high synteny of the helmeted honeyeater genome with that of 3 passerine species (e.g., 32 Hi-C scaffolds mapped to 30 zebra finch autosomes and Z chromosome). The genome assembly and linkage map suggest that the helmeted honeyeater exhibits a fission of chromosome 1A into 2 chromosomes relative to zebra finch. PSMC analysis showed a ∼15-fold decline in effective population size to ∼60,000 from mid- to late Pleistocene.ConclusionsThe annotated chromosome-length genome and high-density linkage map provide rich resources for evolutionary studies and will be fundamental in guiding conservation efforts for the helmeted honeyeater.

Lifetime Fitness Costs of Inbreeding and Being Inbred in a Critically Endangered Bird

Reduced fitness as a result of inbreeding is a major threat facing many species of conservation concern [1-4]. However, few case studies for assessing the magnitude of inbreeding depression in the wild means that its relative importance as a risk factor for population persistence remains under-appreciated [5]. The increasing availability and affordability of genomic technologies provide new opportunities to address knowledge gaps around the magnitude and manifestation of inbreeding depression in wild populations [6-12]. Here, we combine over three decades of individual lifetime reproductive data and genomic data to estimate the relative lifetime and short-term fitness costs of both being inbred and engaging in inbreeding in the last wild population (<250 individuals remaining) of an iconic and critically endangered bird: the helmeted honeyeater Lichenostomus melanops cassidix. The magnitude of inbreeding depression was substantial: the mean predicted lifetime reproductive success of the most inbred (homozygosity= 0.82) individuals was on average 87%-90% lower than that ofthe least inbred (homozygosity= 0.75). For individual reproductive events and lifetime measures, we provide rare empirical evidence that pairing with a genetically dissimilar individual can reduce fitness costs associated with being an inbred individual. By comparing lifetime and short-term fitness measures, we demonstrate how short-term measures of reproductive success that are associated with only weak signatures of inbreeding depression can still underlie stronger lifetime effects. Our study represents a valuable case study, highlighting the critical importance ofinbreeding depression as a factor influencing the immediate viability of populations in threatened species management.

Scope for genetic rescue of an endangered subspecies though re-establishing natural gene flow with another subspecies.

Genetic diversity is positively linked to the viability and evolutionary potential of species but is often compromised in threatened taxa. Genetic rescue by gene flow from a more diverse or differentiated source population of the same species can be an effective strategy for alleviating inbreeding depression and boosting evolutionary potential. The helmeted honeyeater Lichenostomus melanops cassidix is a critically endangered subspecies of the common yellow-tufted honeyeater. Cassidix has declined to a single wild population of ~130 birds, despite being subject to intensive population management over recent decades. We assessed changes in microsatellite diversity in cassidix over the last four decades and used population viability analysis to explore whether genetic rescue through hybridization with the neighbouring Lichenostomus melanops gippslandicus subspecies constitutes a viable conservation strategy. The contemporary cassidix population is characterized by low genetic diversity and effective population size (N(e) < 50), suggesting it is vulnerable to inbreeding depression and will have limited capacity to evolve to changing environments. We find that gene flow from gippslandicus to cassidix has declined substantially relative to pre-1990 levels and argue that natural levels of gene flow between the two subspecies should be restored. Allowing gene flow (~4 migrants per generation) from gippslandicus into cassidix (i.e. genetic rescue), in combination with continued annual release of captive-bred cassidix (i.e. demographic rescue), should lead to positive demographic and genetic outcomes. Although we consider the risk of outbreeding depression to be low, we recommend that genetic rescue be managed within the context of the captive breeding programme, with monitoring of outcomes.

Dispatches

Dispatches

Estimating wildlife population trends: the case of the Helmeted Honeyeater

Assessing trends in wildlife populations involves estimating whether those populations are stable, increasing or decreasing, and trends can infer the success or failure of management. This paper determines trends in a population of critically endangered Helmeted Honeyeaters (Lichenostomus melanops cassidix) in Victoria, Australia, using a range of estimation procedures. Analyses of breeding pairs data show the population of Helmeted Honeyeaters increased, with an annual finite growth rate (λ) of 1.07 (95% confidence intervals 1.02-1.12), over 8 years (1989–90 to 1996–97) then decreased over 12 years (1997–98 to 2008–09) with λ of 0.94 (95% CI 0.91-0.96). Demographic analysis estimated that during the first 8 years λ was 1.21 (95% CI 1.01-1.40), which overlapped the estimate of λ from breeding pairs data but was less precise. There were no demographic data for the later period of 12 years. The number of breeding pairs in 1 year was positively, although only weakly (R2 = 0.23), and significantly (P = 0.03) related to annual rainfall 2 years prior. Wildlife management, such as that of Helmeted Honeyeaters, needs ongoing, quantitative assessment of trends involving measures such as λ, with associated 95% CI.

Integrating phylogeography and morphometrics to assess conservation merits and inform conservation strategies for an endangered subspecies of a common bird species

Understanding the evolutionary history of threatened populations can improve their conservation management. Re-establishment of past but recent gene flow could re-invigorate threatened populations and replenish genetic diversity, necessary for population persistence. One of the four nominal subspecies of the common yellow-tufted honeyeater, Lichenostomus melanops cassidix, is critically endangered despite substantial conservation efforts over 55years. Using a combination of morphometric, genetic and modeling approaches we tested for its evolutionary distinctiveness and conservation merit. We confirmed that cassidix has at least one morphometric distinction. It also differs genetically from the other subspecies in allele frequencies but not phylogenetically, implying that its evolution was recent. Modeling historical distribution supported a lack of vicariance and suggested possible gene flow among subspecies at least since the late Pleistocene. Multi-locus coalescent analyses indicated that cassidix diverged from its common ancestor with neighboring subspecies gippslandicus sometime from the mid-Pleistocene to the Holocene, and that it has the smallest historical effective population size of all subspecies. It appears that cassidix diverged from its ancestor with gippslandicus through a combination of drift and local selection. From patterns of genetic subdivision on two spatial scales and morphological variation we concluded that cassidix, gippslandicus and (melanops+meltoni) are diagnosable as subspecies. Low genetic diversity and effective population size of cassidix may translate to low genetic fitness and evolutionary potential, accordingly we recommend managed gene flow from gippslandicus (with which it can be inferred to have recently experienced natural gene flow) to favor recovery of cassidix.

Use of spider silk for nest building by the Regent HoneyeaterAnthochaera phrygiaand the Helmeted HoneyeaterLichenostomus melanops cassidix

The Regent Honeyeater Anthochaera phrygia and Helmeted Honeyeater Lichenostomus melanops cassidix have both suffered a dramatic decline in number and reduction in range as a result of extensive habitat clearance. As part of recovery plans aimed toward reintroduction to the wild, both species are part of an intensive captive breeding program being conducted at a number of institutions, including Taronga Zoo, Sydney. These honeyeaters incorporate arthropod silk into their nests, as has been reported for other small passerines. However, little is known about how birds choose and use the silk that they collect during nest building. We presented breeding pairs with cribellate silk from the Black House Spider Badumna sp. and ecribellate silk from the Golden Orb-weaver Nephila plumipes or ‘clean/fresh’ and ‘dirty/old’ Badumna sp. silk and observed which were taken by the birds. Lichenostomus melanops cassidix showed a preference for the cribellate silk of Badumna sp., always selecting this silk type first. Never...

Demography of the Helmeted Honeyeater (Lichenostomus melanops cassidix)

Understanding the demography of threatened taxa is essential for formulating effective management strategies for their conservation and for making predictions about their long-term prospects. With fewer than 25 breeding pairs in the current wild population, the Helmeted Honeyeater (Lichenostomus melanops cassidix) is one of the most threatened birds in Australia. Demography of the sole wild population of the Helmeted Honeyeater was investigated by monitoring 526 nests between 1984 and 1996 and 324 colour-banded birds between 1984 and 2008. Throughout the study, the population was effectively closed, there being no evidence of immigration or emigration. Mean survivorship of nests from laying to fledging was 0.17, and mean survivorship of juveniles (from 40 days to 1 year of age) was 0.63. Weighted mean annual survivorship of adult females and males was 0.75 and 0.81 respectively. The population showed little between-year variation in annual productivity and survivorship, with sufficient recruitment for positive population growth. In general, the population dynamics of the Helmeted Honeyeater fit the pattern of an ‘old endemic’ Australian passerine, with low survival of eggs and chicks, extended parental care of juveniles and high survivorship of juveniles and adults. Eggs and chicks that would not naturally survive are a resource that may be used to assist recovery of the population.

Optimal Marking of Threatened Species to Balance Benefits of Information with Impacts of Marking

Marking animals so that they are uniquely identifiable provides information that may assist conservation efforts. Nevertheless, some methods used to mark animals can be harmful. We used mathematical methods to assess the trade-off between the impact of marking threatened species and the value of the information gained. We considered the case where 2 management strategies, each aiming to improve a species' survival rate, are implemented in an experimental phase. The results of the experiment were applied in a postexperimental management phase. We expressed the expected number of survivors in both phases mathematically, accounting for any mortality caused by the experiment, and determined the proportion of animals to mark to maximize this number. The optimal number of animals to mark increased with the number of individuals available for the experiment and with the number of individuals to be managed in the future. The optimal solution was to mark only 25% of the animals when there were 1000 individuals available for the experiment, the results were used to manage 2000 individuals, and marking caused mortality of 1%. Fewer animals were marked when there were fewer animals in either phase or when marking caused higher mortality. In the case of the Helmeted Honeyeater (Lichenostomus melanops cassidix), the optimal proportion to mark was <1 if the mortality rate was >0.15%-1%, with the threshold depending on the number of animals in the experimental and postexperimental phases. The trade-off between gaining more information about a species and possibly harming individuals of that species by marking them is difficult to assess subjectively. We show how to determine objectively the optimal proportion of animals to mark to enhance the management of threatened species.

The effects of climate on breeding in the Helmeted Honeyeater

Climate is known to influence the timing and success of breeding in many bird species. In the northern hemisphere, significant breeding changes have been associated with climate change, with warming temperatures, often, but not always, corresponding to earlier laying. For the critically endangered Helmeted Honeyeater (Lichenostomus melanops cassidix) of central southern Victoria, Australia, climate also plays a role in the timing and success of breeding. During the period 1989 to 2006, the timing of laying became earlier and there was a possible reduction in the mean number of eggs laid per breeding season. These changes correspond to a reduction in rainfall and mild warming. If these trends continue under projected climate-change regimes, there will be increased risk of further population decline.

Accounting for Management Costs in Sensitivity Analyses of Matrix Population Models

Traditional sensitivity and elasticity analyses of matrix population models have been used to inform management decisions, but they ignore the economic costs of manipulating vital rates. For example, the growth rate of a population is often most sensitive to changes in adult survival rate, but this does not mean that increasing that rate is the best option for managing the population because it may be much more expensive than other options. To explore how managers should optimize their manipulation of vital rates, we incorporated the cost of changing those rates into matrix population models. We derived analytic expressions for locations in parameter space where managers should shift between management of fecundity and survival, for the balance between fecundity and survival management at those boundaries, and for the allocation of management resources to sustain that optimal balance. For simple matrices, the optimal budget allocation can often be expressed as simple functions of vital rates and the relative costs of changing them. We applied our method to management of the Helmeted Honeyeater (Lichenostomus melanops cassidix; an endangered Australian bird) and the koala (Phascolarctos cinereus) as examples. Our method showed that cost-efficient management of the Helmeted Honeyeater should focus on increasing fecundity via nest protection, whereas optimal koala management should focus on manipulating both fecundity and survival simultaneously. These findings are contrary to the cost-negligent recommendations of elasticity analysis, which would suggest focusing on managing survival in both cases. A further investigation of Helmeted Honeyeater management options, based on an individual-based model incorporating density dependence, spatial structure, and environmental stochasticity, confirmed that fecundity management was the most cost-effective strategy. Our results demonstrate that decisions that ignore economic factors will reduce management efficiency.

Assessing programs for monitoring threatened species - a tale of three honeyeaters (Meliphagidae)

We critically evaluated population-monitoring programs for three endangered species of Australian honeyeater: the helmeted honeyeater, Lichenostomus melanops cassidix, the black-eared miner, Manorina melanotis, and the regent honeyeater, Xanthomyza phrygia (Meliphagidae). Our results challenge the common assumption that meaningful monitoring is possible in all species within the five-year lifetime of recovery plans. We found that the precision achievable from monitoring programs not only depends on the monitoring technique applied but also on the species' biology. Relevant life-history attributes include a species' pattern of movement, its home-range size and its distribution. How well understood and predictable these attributes are will also influence monitoring precision. Our results highlight the large degree of variability in precision among monitoring programs and the value of applying power analysis before continuing longer-term studies. They also suggest that managers and funding agencies should be mindful that more easily monitored species should not receive preferential treatment over species that prove more difficult to monitor.

Thiamine Deficiency in Honeyeaters

Twelve helmeted honeyeaters (Lichenostomus melanops cassidix), 11 yellow-tufted honeyeaters (Lichenostomus melanops gippslandica), 3 purple-crowned lorikeets (Glossopsitta porphyrocephala), and 3 little lorikeets (Glossopsitta pusilla) died over a short period of time with acute thiamine deficiency. Diagnosis was based on polioencephalomalacia observed histologically, low brain thiamine levels (<1 mg/kg), and the absence of other significant findings on tests performed. The birds were maintained on an artificial nectar (water, honey, and a multivitamin supplement) for 2 years, but this diet was analyzed to be low in thiamine (0.001 mg thiamine/ml of diet). An additional secondary thiamine antagonist, not identified, may have precipitated the mass mortality.

Vegetation of the Yellingbo Nature Conservation Reserve and its relationship to the distribution of the helmeted honeyeater, bell miner and white-eared honeyeater

The structural characteristics of the habitat of the helmeted honeyeater, Lichenostomus melanops cassidix, the bell miner, Manorina melanophrys, and the white-eared honeyeater, Lichenostomus leucotis, within the Yellingbo Nature Conservation Reserve have been described elsewhere. The present study aimed to describe the floristic characteristics of the reserve, and explore the relationship between the floristic composition of the vegetation and the presence of each of the three honeyeater species. Six vegetation groups were described and mapped for the reserve. The bell miner and white-eared honeyeater were found to occupy all vegetation groups in proportion to their availability. The helmeted honeyeater was strongly associated with only one of the vegetation groups: E. camphora open forest. The helmeted honeyeater therefore appears to be the most floristically restricted of the three honeyeater species, and this dependence may lead to greater levels of competition for habitat with the more generalist bell miner and white-eared honeyeater.

Annual cycle of the Helmeted Honeyeater Lichenostomus melanops cassidix, a sedentary inhabitant of a predictable environment

The annual cycle of breeding, moult and weight variation in the Helmeted HoneyeaterLichenostomus melanops cassidix, a sedentary bird of temperate southeast Australia, is documented. Breeding and moult were sequential unimodal annual events, whose timing was highly consistent between years. However, overlap of breeding and moult was frequent, and some individuals even commenced primary moult before laying their final clutch. The timing of the post‐juvenile moult was coincident with that of adults. Early‐hatched young moulted within a few months of hatching, but late‐hatched young deferred moult for a year. Helmeted Honeyeaters were heaviest in autumn and early winter, and lightest in spring and early summer, a cycle most consistent with the redirection of all available resources to reproduction. The long breeding season (seven‐and‐a‐half months) of the Helmeted Honeyeater, extensive overlap of breeding and moult, and other life‐history attributes including small clutch size, are more consistent with the described bio‐rhythmic patterns for birds in the humid tropics than the temperate zone. However, the Helmeted Honeyeater has a fairly rapid primary moult rate, unusual amongst species that overlap moult and breeding. This combination of attributes reflects the stable, somewhat seasonal environment occupied and the resource monopoly established by this tightly territorial subspecies. We speculate that extension of the breeding season, by overlapping breeding and moult, is one of the few options available to vary life‐history strategies amongst ‘old‐endemic’ Australian birds of the temperate zone.

Bioclimatic Analysis to Enhance Reintroduction Biology of the Endangered Helmeted Honeyeater (Lichenostomus melanops cassidix) in Southeastern Australia

Reintroduction programs are a high‐risk conservation strategy for restoring populations of endangered species. The success of these programs often depends on the ability to identify suitable habitat within the species’ former range. Bioclimatic analysis offers an empirical, explicit, robust, and repeatable method to analyze large areas rapidly using a small number of locality records, and in turn predicting (and/or reconstructing) its potential distribution limits. This approach therefore can estimate the broad limits of the distribution of a taxon, using data that may be inadequate for standard forms of statistical analysis. We illustrate the potential value of bioclimatic modeling for reintroduction biology using a case study of the highly endangered Helmeted Honeyeater (Lichenostomus melanops cassidix) from Victoria, southeastern Australia. The results of our analyses assisted us to both predict the former range limits of the Helmeted Honeyeater and determine the broad limits of those areas that may contain potentially suitable sites for future reintroduction programs for the subspecies. The analysis predicted that the range of the Helmeted Honeyeater extends from the Yarra River district east of Melbourne, south to the Western Port Bay and east as far as the Morwell area of Victoria. The climatic characteristics of habitat occupied by the extant population of the Helmeted Honeyeater were found to be unique within its predicted range. We recommend that reintroduction efforts therefore be concentrated within this small area, as has occurred to date.

A study of Resource Partitioning Within the Helmeted Honeyeater Lichenostomus melanops cassidix During the Non-breeding Season

SummaryIntraspecific variation in resource partitioning was evaluated in the Helmeted Honeyeater Lichenostomus melanops cassidix according to age, sex and breeding status during the 1994 non-breeding season. The home ranges of males and females within a breeding pair were highly overlapping, of similar size (males: X = 0.32 ± 0.07 ha; females: X = 0.26 ± 0.04 ha) and did not differ significantly in vegetational composition. Breeding adults and their juvenile off-spring also had similar-sized, highly overlapping home ranges. For one juvenile the degree of overlap decreased markedly as the bird matured. Non-breeding adults tended to occupy different vegetation communities to those inhabited by breeding adults. Male breeding adults spent significantly more time in the canopy stratum than females, who were observed more frequently in the lower strata. Both juveniles and non-breeding adults spent less time in the canopy than breeding adults. Analysis of activity budgets did not reveal specialised foraging behaviour according to height in the vegetation, or seasonal change from autumn to winter. Male and female Helmeted Honeyeaters showed similar levels of aggression when present in the canopy region. The distribution of manna points was random at Green site, but occurred in areas with little tea-tree understorey at Mauve site.

Extinction dynamics of the helmeted honeyeater: effects of demography, stochasticity, inbreeding and spatial structure

HEAVAN is a computer-based model of the last remaining population of helmeted honeyeaters ( Lichenostomus melanops cassidix). It models a population structured according to sex and breeding status, and incorporates spatial structure, environmental stochasticity, demographic stochasticity, catastrophes, and inbreeding effects. The purpose of this model is to identify options for the management of this extremely rare and endangered bird. The model predicts that there is an appreciable risk of decline within the next 50 years. Sensitivity analysis indicates that the helmeted honeyeater is vulnerable to catastrophes such as fire, and the results are particularly sensitive to estimates of the level of random fluctuations in survivorships.