Low genetic diversity in the bottlenecked population of endangered non-native banteng in northern Australia

Undomesticated (wild) banteng are endangered in their native habitats in Southeast Asia. A potential conservation resource for the species is a large, wild population in Garig Gunak Barlu National Park in northern Australia, descended from 20 individuals that were released from a failed British outpost in 1849. Because of the founding bottleneck, we determined the level of genetic diversity in four subpopulations in the national park using 12 microsatellite loci, and compared this to the genetic diversity of domesticated Asian Bali cattle, wild banteng and other cattle species. We also compared the loss of genetic diversity using plausible genetic data coupled to a stochastic Leslie matrix model constructed from existing demographic data. The 53 Australian banteng sampled had average microsatellite heterozygosity (HE) of 28% compared to 67% for outbred Bos taurus and domesticated Bos javanicus populations. The Australian banteng inbreeding coefficient (F) of 0.58 is high compared to other endangered artiodactyl populations. The 95% confidence bounds for measured heterozygosity overlapped with those predicted from our stochastic Leslie matrix population model. Collectively, these results show that Australian banteng have suffered a loss of genetic diversity and are highly inbred because of the initial population bottleneck and subsequent small population sizes. We conclude that the Australian population is an important hedge against the complete loss of wild banteng, and it can augment threatened populations of banteng in their native range. This study indicates the genetic value of small populations of endangered artiodactyls established ex situ.     

Using carbon isotope analysis of the diet of two introduced Australian megaherbivores to understand Pleistocene megafaunal extinctions

Aim Australia lost a diverse assemblage of large marsupial herbivores in the late Pleistocene, with suggestions that the extinctions were biased towards browsers. In modern times two bovines, the Asian water buffalo (Bubalus bubalis) and banteng (Bos javanicus), have established feral populations in the Northern Territory, Australia. Buffalo have aggressively expanded throughout the savanna landscape, yet banteng remain near their point of introduction on the Cobourg Peninsula. We hypothesized that this difference is related to feeding ecology, possibly reflecting a legacy of the Pleistocene extinctions. Location Western Arnhem Land, Northern Territory, Australia. Methods Analysing a previously published dataset of body mass and feeding ecology of extinct and extant marsupial herbivores, we evaluated whether browsers were at greater risk of extinction than grazers. We compared the carbon isotope composition and nitrogen content of banteng and buffalo dung in order to evaluate the hypotheses that the differences in invasion success are related to feeding ecology, and that seasonal variation in browse consumption is linked to changing nutritional quality of grass. Results Controlling for body mass, the Pleistocene extinctions were clearly biased towards browsers. Introduced banteng appear to be primarily browsers, with their diets comprising 40% grass in the wet season and 15% in the late dry season. Buffalo have a more variable diet, with an increasing proportion of browse from the wet (30%) to the late dry season (75%), and can therefore be described as switching from grazer to browser. The decline of grass in the diet of both species appears to reflect the decline in the nutritional value of grass through the dry season, an inference supported by the negative relationship between δ¹³C values and the nitrogen content of dung. Main conclusions Banteng and buffalo are much larger than extant native herbivores, of which browsers are restricted to isolated rocky habitats. This suggests that banteng and buffalo have filled niches made vacant following the Pleistocene extinctions. The success of buffalo appears to be related to their greater dietary breadth, which enables them to graze and browse in eucalypt savannas, whilst the browsing banteng remain tethered to a mosaic of rain forest patches. The restriction of browsers may be a long‐range consequence of habitat transformations associated with Aboriginal landscape burning.     

Mutualism vs. antagonism in introduced and native ranges: Can seed dispersal and predation determine Acacia invasion success?

Plant species introduced to new regions can escape their natural enemies but may also lose important mutualists. While mutualistic interactions are often considered too diffuse to limit plant invasion, few studies have quantified the strength of interactions in both the native and introduced ranges, and assessed whether any differences are linked to invasion outcomes. For three Acacia species adapted for ant dispersal (myrmecochory), we quantified seed removal probabilities associated with dispersal and predation in both the native (Australian) and introduced (New Zealand) ranges, predicting lower removal attributable to dispersal in New Zealand due to a relatively depauperate ant fauna. We used the role of the elaiosome to infer myrmecochory, and included treatments to measure vertebrate seed removal, since this may become an important determinant of seed fate in the face of reduced dispersal. We then tested whether differences in seed removal patterns could explain differences in the invasion success of the three Acacia species in New Zealand.Overall seed removal by invertebrates was lower in New Zealand relative to Australia, but the difference in removal between seeds with an elaiosome compared to those without was similar in both countries. This implies that the probability of a removed seed being dispersed by invertebrates was comparable in New Zealand to Australia. The probability of seed removal by vertebrates was similar and low in both countries. Differences in the invasive success of the three Acacia species in New Zealand were not explained by differences in levels of seed predation or the strength of myrmecochorous interactions. These findings suggest that interactions with ground foraging seed predators and dispersers are unlikely to limit the ability of Acacia species to spread in New Zealand, and could not explain their variable invasion success.     

Reintroduction of locally extinct vertebrates impacts arid soil fungal communities

Introduced species have contributed to extinction of native vertebrates in many parts of the world. Changes to vertebrate assemblages are also likely to alter microbial communities through coextinction of some taxa and the introduction of others. Many attempts to restore degraded habitats involve removal of exotic vertebrates (livestock and feral animals) and reintroduction of locally extinct species, but the impact of such reintroductions on microbial communities is largely unknown. We used high‐throughput DNA sequencing of the fungal internal transcribed spacer I (ITS1) region to examine whether replacing exotic vertebrates with reintroduced native vertebrates led to changes in soil fungal communities at a reserve in arid central Australia. Soil fungal diversity was significantly different between dune and swale (interdune) habitats. Fungal communities also differed significantly between sites with exotic or reintroduced native vertebrates after controlling for the effect of habitat. Several fungal operational taxonomic units (OTUs) found exclusively inside the reserve were present in scats from reintroduced native vertebrates, providing a direct link between the vertebrate assemblage and soil microbial communities. Our results show that changes to vertebrate assemblages through local extinctions and the invasion of exotic species can alter soil fungal communities. If local extinction of one or several species results in the coextinction of microbial taxa, the full complement of ecological interactions may never be restored.     

What is the taxonomic status of the Cambodian banteng and does it have close genetic links with the kouprey?

In a recent paper, Galbreath, Mordacq & Weiler (2006) concluded that the kouprey Bos sauveli was not a natural species, but rather a feral animal derived from hybridization between banteng Bos javanicus and zebu Bos taurus indicus . Here, we analyze two mitochondrial genes (cytochrome b and subunit II of the cytochrome c oxidase) for all the seven species of the subtribe Bovina, including new sequences for several specimens of banteng, zebu and gaur of Cambodia. Our analyses indicate that mitochondrial sequences of Cambodian banteng are divergent from those of Javan banteng (mean difference =4.27%), but similar to those of kouprey (1.25%). We propose two conflicting hypotheses to interpret these results: (1) the Cambodian and Indonesian banteng belong to two distinct species, and the kouprey derived from Cambodian banteng; (2) all subspecies of banteng belong to Bo. javanicus , but the mitochondrial genome of kouprey was transferred by natural hybridization into the ancestor of Cambodian banteng. Morphological, ecological and ethological characteristics of banteng and kouprey rather support the second hypothesis. However, we need to sequence nuclear markers, and to analyze banteng from Lao, Myanmar, Thailand and Vietnam, to give a definitive conclusion on the taxonomic status of banteng and kouprey.     

Controlling vertebrate pests with fluoroacetate: lessons in wildlife management,bio-ethics,and co-evolution

The uses of sodium monofluoroacetate (compound 1080) as a vertebrate predacide in the USA and Australia are reviewed. The US applications centre on control of native species, while many of Australia's vertebrate pests are introduced species. This, coupled with the natural resistance of some Australian native fauna to 1080, has contributed to different patterns of use in both countries and different public attitudes to control programmes. The 1080 case corrects the omission of vertebrate pest control examples from the discussions of pest control in school biology texts, and highlights the interplay of economics, public opinion, bio-ethics, and biological principles in pest control programmes. Exercises on scientific vs emotive writing, data presentation, and co-evolution in Australia are suggested as possible curriculum extension exercises.     

Vertebrate browsing impacts in a threatened montane plant community and implications for management

Montane ecosystems are vulnerable to the removal of vegetation cover through browsing by feral or native vertebrate fauna. The highest elevated peaks of the Stirling Range in Western Australia provide habitat for an endemic plant community, Critically Endangered due to plant disease, frequent fire and an emerging threat of browsing by vertebrate fauna. Survey and camera trapping confirmed the herbivorous feral Rabbit (Oryctolagus cuniculus) and native Quokka (Setonix brachyurus) are present. Dietary analysis through faecal examination revealed contrasting diets and implicates native rather than feral species as responsible for impacts on dicotyledonous species, and in particular those of conservation significance. Exclosure experiments conducted over 1 year revealed significant changes in abundance, cover and height of perennial herbs and an increase in growth and/or reproduction of four threatened endemic plants. Detrimental impacts caused by native browsing fauna are not unprecedented and may be attributed to disequilibria in ecosystem processes due to multiple interacting threats. Montane ecosystems may be particularly vulnerable to browsing due to their naturally slow recovery after disturbance and browsing may also create environmental conditions more conducive to plant disease. For plant species with critically low population numbers, the impact of browsing poses a threat to population persistence and undermines investment into other conservation recovery actions. For effective management, it is critical to determine the relative impact of browsing species present. Where native species are implicated, the physical protection of high value assets in wire exclosures is warranted to complement other recovery actions and ensure effective species and community recovery.     

Growth, body condition and demography of wild banteng (Bos javanicus) on Cobourg Peninsula, northern Australia

Growth, body condition and demography of a sample of 125 banteng, Bos javanicus , from a largely unharvested wild herd on Cobourg Peninsula in northern Australia were examined. Growth (measured as changes in age-specific head-length) was sexually dimorphic, males growing faster and attaining larger sizes than females. Females reached maximum size in three to four years, and males in five to six years. Body condition (measured by the kidney-fat index) was low amongst juveniles, increasing into middle age. Condition of aged females showed a marked decline. Males attained sexual maturity between three and four years, females between two and four years. Fecundity declined in older females. Breeding was seasonal, mating activity peaking during October and November, with births most frequent between June and August. Mortality amongst calves was high over the first six months of life, declining rapidly amongst older animals. Comparison of demographic data with those reported for captive herds indicates that the wild banteng in this study matured later, were less fecund, and suffered a higher rate of juvenile mortality. Lower fecundity and higher juvenile mortality were associated with patterns of age-specific body condition, suggesting that food availability was the major factor affecting demography and hence rates of change in banteng abundance.     

Resolving a zoological mystery: the kouprey is a real species

The kouprey is a rare and enigmatic forest ox discovered by scientists in Cambodia only in 1937. Numerous morphological hypotheses have been proposed for the origin of the kouprey: that it is a species closely related to banteng and gaur, two other wild oxen of southeast Asia; a morphologically divergent species placed in a separate genus, named Novibos; a wild species linked to aurochs and domestic cattle; a vicariant population of banteng; a feral cattle; or a hybrid of banteng with either zebu cattle, gaur or water buffalo. In a recent paper, which gained a lot of media coverage, Galbreath et al. analysed mitochondrial DNA sequences and concluded that the kouprey never existed as a wild, natural species, and that it was a feral hybrid between banteng and zebu cattle. Here we analyse eight DNA markers-three mitochondrial regions and five nuclear fragments-representing an alignment of 4582 nucleotides for the holotype of the kouprey and all related species. Our results demonstrate that the kouprey is a real and naturally occurring species, and show that Cambodian populations of banteng acquired a mitochondrial genome of kouprey by natural introgressive hybridization during the Pleistocene epoch.     

Keystone effects of an alien top-predator stem extinctions of native mammals

Alien predators can have catastrophic effects on ecosystems and are thought to be much more harmful to biodiversity than their native counterparts. However, trophic cascade theory and the mesopredator release hypothesis predict that the removal of top predators will result in the reorganization of trophic webs and loss of biodiversity. Using field data collected throughout arid Australia, we provide evidence that removal of an alien top-predator, the dingo, has cascading effects through lower trophic levels. Dingo removal was linked to increased activity of herbivores and an invasive mesopredator, the red fox (Vulpes vulpes), and to the loss of grass cover and native species of small mammals. Using species distribution data, we predict that reintroducing or maintaining dingo populations would produce a net benefit for the conservation of threatened native mammals across greater than 2.42 × 10⁶ km² of Australia. Our study provides evidence that an alien top predator can assume a keystone role and be beneficial for biodiversity conservation, and also that mammalian carnivores more generally can generate strong trophic cascades in terrestrial ecosystems.     

Rapid recovery of mammal fauna in the central Kimberley,northern Australia,following the removal of introduced herbivores

Australia has lost more native mammal species than any other country in the past two centuries, and this record of loss looks likely to worsen over the next few decades. Small‐ to medium‐sized mammals are declining in both distribution and density across large tracts of northern Australia's tropical savannas, including within protected areas. The most likely causes are a combination of changed fire patterns, the impacts of introduced herbivores and predation by feral cats. Here, in contrast to the prevailing trend across northern Australia, we report the recovery of native mammals in response to a large‐scale (>40 000 ha) destocking experiment carried out at Mornington Wildlife Sanctuary in the central Kimberley, north‐west Australia. Following the removal of introduced herbivores from 2004, the species richness and abundance of small native rodents and dasyurids increased significantly across all sampled habitats over the next 3 years. We discuss the implications of these results for guiding land management and applied research to help to reduce the impending risk of mammalian extinctions in northern Australia.     

Excretion patterns of fluid and different sized particle passage markers in banteng (Bos javanicus) and pygmy hippopotamus (Hexaprotodon liberiensis): two functionally different foregut fermenters

Processing of ingesta particles plays a crucial role in the digestive physiology of herbivores. In the ruminant forestomach different sized particles are stratified into a small and a large particle fraction and only the latter is regurgitated and remasticated to smaller, easier-to-digest particles. In contrast, it has been suggested that in non-ruminating foregut fermenters, such as hippopotamuses, larger particles should be selectively excreted since they tend to be digested at a slower rate and hence can be considered intake-limiting bulk. In our study we determined the mean retention time (MRT) of fluids and different sized particles (2 mm and 10 mm) in six pygmy hippos (Hexaprotodon liberiensis) and six banteng (Bos javanicus) on a diet of fresh grass at two intake levels. We used cobalt ethylendiamintetraacetate (Co-EDTA) as fluid and chromium (Cr)-mordanted fibre (2 mm) and cerium (Ce)-mordanted fibre (10 mm) as particle markers, mixed in the food. Average total tract MRT for fluid, small and large particles at the high intake level was 32, 76 and 73 h in pygmy hippos and 25, 56 and 60 h in banteng, and at the low intake level 39, 109, and 105 h in pygmy hippos and 22, 51 and 58 h in banteng, respectively. In accordance with the prediction, large particles moved faster than, or as fast as the small particles, through the gut of pygmy hippos. In contrast, large particles were excreted slower than the small particles in the ruminant of this study, the banteng. Pygmy hippos had longer retention times than the banteng, which probably compensate for the less efficient particle size reduction. Although the results were not as distinct as expected, most likely due to the fact that ingestive mastication of the larger particle marker could not be prevented, they confirm our hypothesis of a functional difference in selective particle retention between ruminating and non-ruminating foregut fermenters.     

Top predators as biodiversity regulators: the dingo Canis lupus dingo as a case study

Top‐order predators often have positive effects on biological diversity owing to their key functional roles in regulating trophic cascades and other ecological processes. Their loss has been identified as a major factor contributing to the decline of biodiversity in both aquatic and terrestrial systems. Consequently, restoring and maintaining the ecological function of top predators is a critical global imperative. Here we review studies of the ecological effects of the dingo Canis lupus dingo, Australia's largest land predator, using this as a case study to explore the influence of a top predator on biodiversity at a continental scale. The dingo was introduced to Australia by people at least 3500 years ago and has an ambiguous status owing to its brief history on the continent, its adverse impacts on livestock production and its role as an ecosystem architect. A large body of research now indicates that dingoes regulate ecological cascades, particularly in arid Australia, and that the removal of dingoes results in an increase in the abundances and impacts of herbivores and invasive mesopredators, most notably the red fox Vulpes vulpes. The loss of dingoes has been linked to widespread losses of small and medium‐sized native mammals, the depletion of plant biomass due to the effects of irrupting herbivore populations and increased predation rates by red foxes. We outline a suite of conceptual models to describe the effects of dingoes on vertebrate populations across different Australian environments. Finally, we discuss key issues that require consideration or warrant research before the ecological effects of dingoes can be incorporated formally into biodiversity conservation programs.     

Banteng (Bos javanicus) embryos and pregnancies produced by interspecies nuclear transfer

The banteng (Bos javanicus), a member of the bovidae family, is currently listed as threatened by the IUCN Red List and it is estimated the total world population is <10,000 animals. In exotic or endangered species, the lack of oocytes and recipients precludes the use of traditional somatic cell nuclear transfer (NT), and an approach such as interspecies NT may be the only alternative to produce embryos and offspring. A total of 348 enucleated domestic bovine oocytes were reconstructed with either male (Treatment A) or female (Treatment B) adult banteng fibroblasts and a total of 103 bovine oocytes were parthenogenically activated as a control (Treatment C). There was no significant difference in fusion rate (68 versus 77%) between Treatments A and B. Of fused couplets, those in Treatment A had greater (P < 0.05) cleavage (67 versus 51%) and blastocyst (28 versus 15%) rate than Treatment B. Of a total of 24 blastocysts transferred into 12 domestic cattle recipients from Treatment A, two pregnancies (17%) were established with heart beats detectable at 30 day by rectal ultrasonography. No pregnancies resulted from the transfer of 14 blastocysts from Treatment B. Both pregnancies were subsequently lost, one between 30 and 60 days and the second between 60 and 90 days of gestation. The bovine cytoplast supported mitotic cleavage of banteng karyoplasts, and was capable of reprogramming the nucleus to achieve blastocyst stage embryos and pregnancies in exotic bovids.     

Pollution reduces native diversity and increases invader dominance in marine hard-substrate communities

Anthropogenic disturbance is considered a risk factor in the establishment of non‐indigenous species (NIS); however, few studies have investigated the role of anthropogenic disturbance in facilitating the establishment and spread of NIS in marine environments. A baseline survey of native and NIS was undertaken in conjunction with a manipulative experiment to determine the effect that heavy metal pollution had on the diversity and invasibility of marine hard‐substrate assemblages. The study was repeated at two sites in each of two harbours in New South Wales, Australia. The survey sampled a total of 47 sessile invertebrate taxa, of which 15 (32%) were identified as native, 19 (40%) as NIS, and 13 (28%) as cryptogenic. Increasing pollution exposure decreased native species diversity at all study sites by between 33% and 50%. In contrast, there was no significant change in the numbers of NIS. Percentage cover was used as a measure of spatial dominance, with increased pollution exposure leading to increased NIS dominance across all sites. At three of the four study sites, assemblages that had previously been dominated by natives changed to become either extensively dominated by NIS or equally occupied by native and NIS alike. No single native or NIS was repeatedly responsible for the observed changes in native species diversity or NIS dominance at all sites. Rather, the observed effects of pollution were driven by a diverse range of taxa and species. These findings have important implications for both the way we assess pollution impacts, and for the management of NIS. When monitoring the response of assemblages to pollution, it is not sufficient to simply assess changes in community diversity. Rather, it is important to distinguish native from NIS components since both are expected to respond differently. In order to successfully manage current NIS, we first need to address levels of pollution within recipient systems in an effort to bolster the resilience of native communities to invasion.     

Genetically solving a zoological mystery: was the kouprey (Bos sauveli) a feral hybrid?

A famous zoological discovery of the 20th century was that of the kouprey Bos sauveli , a medium-sized ox inhabiting Cambodian forests. The kouprey was suspiciously intermediate between banteng oxen and domestic zebu cattle in its structure. Mitochondrial DNA sequences of mainland banteng are compared here with a published kouprey sequence, and the comparison demonstrates a close relationship. Either the kouprey derives partly from banteng or (less likely) these particular banteng acquired kouprey DNA via recent genetic introgression. The kouprey may have been a feral hybrid form, a descendant of domestic oxen, rather than a natural species.     

The illusion of nature: perception and the reality of natural landscapes,as illustrated by vertebrate fauna in the Northern Territory,Australia

Biomass figures are compared for common native vertebrate species and common non‐native vertebrate species (including fish, amphibian, reptile, bird and mammal species) across the Northern Territory, an area of ostensibly, largely unmodified natural system. The total biomass of the considered non‐native species very substantially surpasses that of the common native vertebrate species considered; hence, the perception that this is a largely intact natural system is, to some extent, an illusion. This preponderance of biomass of non‐native species may help explain the increasing evidence of ecosystem stress and decline of native species. An integrity index based on the relative biomass of native and non‐native species may provide insight into the status and trends of ecological systems across different regions.     

Functional compensation by insular scavengers: the relative contributions of vertebrates and invertebrates vary among islands

When the extinction of some species results in loss of ecosystem functions, other species may be able to compensate for this loss. Functional compensation has recently been observed on islands where species are likely to become extinct; however, few studies have analysed functional compensation by scavengers in insular environments. Here, we investigated the ecosystem functions of vertebrate and invertebrate scavengers on Honshu, the main island of Japan, and offshore islands (four of the Oki Islands). The Oki Islands lack several native vertebrate scavengers (raccoon dogs, boars, martens, and foxes) that are abundant on Honshu. We experimentally placed mouse carcasses on the forest floors of Honshu (12 sites) and the Oki Islands (7 sites on Dōgo, 4 sites on Nishinoshima, 4 sites on Nakanoshima, and 3 sites on Chiburijima) in September–October 2014 and 2015. Nearly all of the mouse carcasses (95–100%) placed on the forest floor disappeared within 1 week. However, the relative importance of vertebrate and invertebrate scavengers varied among islands. Vertebrate and invertebrate scavengers contributed equally on Honshu (carcass removal by vertebrates, 47%), whereas vertebrate scavengers rarely contributed to carcass removal on three of the Oki Islands (carcass removal by vertebrates: 17% on Dōgo, 30% on Nishinoshima, and 5% on Nakanoshima). Consequently, invertebrate scavengers (Nicrophorus burying beetles) functionally compensated for the low species diversity of vertebrate scavengers on the three islands (carcass burial by Nicrophorus beetles, 65–95%). However, on the small island of Chiburijima, introduced raccoon dogs contributed to nearly all of the removals (93%), suggesting that introduced scavengers can compensate for the functional reduction. This functional compensation by scavengers may help stabilise the functions and/or services of scavengers in island environments.     

Immunocontraception of captive exotic species. I. Przewalski's horses (Equus przewalskii) and banteng (Bos javanicus)

A contraceptive vaccine made of porcine zonae pellucidae (PZP) was tested in three Przewalski's mares and five banteng cows. The vaccine antigen consisted of the complete family of glycoproteins of the porcine zona pellucida, including the sperm receptor ZP3. All mares and three of five banteng were inoculated with 2 or 3 i.m. injections of approximately 65 μg of antigen given over a 6 week period. Two other banteng received inoculations of only 35 μg of antigen on the same schedule. Two of the three mares and three of five banteng cows were pregnant at the time of inoculation. No new pregnancies, as a result of postinoculation breedings, occurred among either the mares 36 months after 65 μg antigen inoculations or among the banteng for 24 months after 65 μg inoculations. One postinoculation pregnancy resulted among the two banteng receiving only 35 μg of antigen. Differences in fertility between treated and control mares and between preinoculation and postinoculation reproductive performance of the banteng were significant (P < 0.05). Urinary ovarian steroid metabolites and behavioral observations indicated follicular development and ovulations were occurring among treated mares during the year following PZP inoculations. PZP immunization produced progressively elevated anti-PZP antibodies in both species, which provided contraceptive protection. PZP immunization appears to be an effective form of contraception in both species. © 1995 Wiley-Liss, Inc.