Standard yet unusual mechanisms of long-distance dispersal: Seed dispersal of Corymbia torelliana by bees

Mellitochory, seed dispersal by bees, has been implicated in long-distance dispersal of the tropical rain forest tree, Corymbia torelliana (Myrtaceae). We examined natural and introduced populations of C. torelliana for 4 years to determine the species of bees that disperse seeds, and the extent and distance of seed dispersal. The mechanism of seed dispersal by bees was also investigated, including fruit traits that promote dispersal, foraging behaviour of bees at fruits, and the fate of seeds. The fruit structure of C. torelliana, with seed presented in a resin reward, is a unique trait that promotes seed dispersal by bees and often results in long-distance dispersal. We discovered that a guild of four species of stingless bees, Trigona carbonaria, T. clypearis, T. sapiens, and T. hockingsi, dispersed seeds of C. torelliana in its natural range. More than half of the nests found within 250 m of fruiting trees had evidence of seed transport. Seeds were transported minimum distances of 20-220 m by bees. Approximately 88% of seeds were dispersed by gravity but almost all fruits retained one or two seeds embedded in resin for bee dispersal. Bee foraging for resin peaked immediately after fruit opening and corresponded to a peak of seed dispersal at the hive. There were strong correlations between numbers of seeds brought in and taken out of each hive by bees (r = 0.753-0.992, P < 0.05), and germination rates were 95 ± 5%. These results showed that bee-transported seeds were effectively dispersed outside of the hive soon after release from fruits. Seed dispersal by bees is a non-standard dispersal mechanism for C. torelliana, as most seeds are dispersed by gravity before bees can enter fruits. However, many C. torelliana seeds are dispersed by bees, since seeds are retained in almost all fruits, and all of these are dispersed by bees.

The physiological and behavioral responses of steers to gaseous ammonia in simulated long distance transport by ship.

Ammonia (NH3) can accumulate in high density cattle accommodation during live export shipments and could potentially threaten the animals' health and welfare. The effects of 4 NH3 concentrations, control (<8), 15, 30, and 45 ppm, on the physiology and behavior of steers were recorded. The animals were held for 12 d under a micro-climate and stocking density similar to shipboard conditions experienced on voyages from Australia to the Middle East during the northern hemispheric summer. In bronchoalveolar lavage samples, ammonia increased (P < 0.05) macrophage activity in proportion to NH3 concentration and it increased (P < 0.05) neutrophil percentage at 30 and 45 ppm, indicating active pulmonary inflammation. It also increased (P < 0.05) lacrimation, nasal secretions and coughing, particularly at 45 ppm, indicating that the NH3 was irritating the mucous membranes of the eyes, nasal cavity and respiratory tract. Ammonia had no effect (P > 0.05) on hematological parameters or body weight. Twenty-eight days after exposure to NH3, the steers' pulmonary macrophage activity and neutrophil levels had returned to normal. It was concluded that ammonia concentrations of 30 and 45 ppm induced temporary inflammatory responses which indicate an adverse effect on the welfare of steers.

The global distribution of Banana bunchy top virus reveals little evidence for frequent recent, human-mediated long distance dispersal events

Banana bunchy top virus (BBTV; family Nanoviridae, genus Babuvirus) is a multi-component single-stranded DNA virus, which infects banana plants in many regions of the world, often resulting in large-scale crop losses. Weanalyzed 171 banana leaf samples from fourteen countries and recovered, cloned, and sequenced 855 complete BBTV components including ninety-four full genomes. Importantly, full genomes were determined from eight countries, where previously no full genomes were available (Samoa, Burundi, Republic of Congo, Democratic Republic of Congo, Egypt, Indonesia, the Philippines, and the USA [HI]). Accounting for recombination and genome component reassortment, we examined the geographic structuring of global BBTV populations to reveal that BBTV likely originated in Southeast Asia, that the current global hotspots of BBTV diversity are Southeast Asia/Far East and India, and that BBTV populations circulating elsewhere in the world have all potentially originated from infrequent introductions. Most importantly, we find that rather than the current global BBTV distribution being due to increases in human-mediated movements of bananas over the past few decades, it is more consistent with a pattern of infrequent introductions of the virus to different parts of the world over the past 1,000 years.

Satellite Telemetry and Long-Range Bat Movements.

Background: Understanding the long-distance movement of bats has direct relevance to studies of population dynamics, ecology, disease emergence, and conservation. Methodology/Principal Findings: We developed and trialed several collar and platform terminal transmitter (PTT) combinations on both free-living and captive fruit bats (Family Pteropodidae: Genus Pteropus). We examined transmitter weight, size, profile and comfort as key determinants of maximized transmitter activity. We then tested the importance of bat-related variables (species size/weight, roosting habitat and behavior) and environmental variables (day-length, rainfall pattern) in determining optimal collar/PTT configuration. We compared battery- and solar-powered PTT performance in various field situations, and found the latter more successful in maintaining voltage on species that roosted higher in the tree canopy, and at lower density, than those that roost more densely and lower in trees. Finally, we trialed transmitter accuracy, and found that actual distance errors and Argos location class error estimates were in broad agreement. Conclusions/Significance: We conclude that no single collar or transmitter design is optimal for all bat species, and that species size/weight, species ecology and study objectives are key design considerations. Our study provides a strategy for collar and platform choice that will be applicable to a larger number of bat species as transmitter size and weight continue to decrease in the future.

The risk of pollen-mediated gene flow from exotic Corymbia plantations into native Corymbia populations in Australia

Sectors of the forest plantation industry in Australia are set to expand in the near future using species or hybrids of the spotted gums (Corymbia, Section Politaria). Plantations of these taxa have already been introduced across temperate and subtropical Australia, representing locally exotic introductions from native stands in Queensland and New South Wales. A literature review was undertaken to provide insights into the potential for pollen-mediated gene flow from these plantations into native populations. Three factors suggest that such gene flow is likely; (1) interspecific hybridisation within the genus has frequently been recorded, including between distantly related species from different sections, (2) apparent high levels of vertebrate pollinator activity may result in plantation pollen being moved over hundreds of kilometres, (3) much of the plantation estate is being established among closely related taxa and therefore few barriers to gene flow are expected. Across Australia, 20 of the 100 native Corymbia taxa were found to have regional level co-occurrence with plantations. These were located most notably within regions of north-east New South Wales and south-east Queensland, however, co-occurrence was also found in south-west Western Australia and eastern Victoria. The native species found to have co-occurrence were then assessed for the presence of reproductive barriers at each step in the process of gene flow that may reduce the number of species at risk even further. The available data suggest three risk categories exist for Corymbia. The highest risk was for gene flow from plantations of spotted gums to native populations of spotted gums. This was based on the expected limited existence of pre- and post-zygotic barriers, substantial long-distance pollen dispersal and an apparent broad period of flowering in Corymbia citriodora subsp. variegata plantations. The following risk category focussed on gene flow from Corymbia torelliana × C. c. variegata hybrid plantations into native C. c. variegata, as the barriers associated with the production and establishment of F1 hybrids have been circumvented. For the lowest risk category, Corymbia plantations may present a risk to other non-spotted gum species, however, further investigation of the particular cross-combinations is required. A list of research directions is provided to better quantify these risks. Empirical data will need to be combined within a risk assessment framework that will not only estimate the likelihood of exotic gene flow, but also consider the conservation status/value of the native populations. In addition, the potential impacts of pollen flow from plantations will need to be weighed up against their various economic and environmental benefits.

Stakeholders' assessment of welfare indicators for sheep and cattle exported by sea from Australia

An adaptive conjoint analysis was use to evaluate stakeholders' opinion of welfare indicators for ship-transported sheep and cattle, both onboard and in pre-export depots. In consultations with two nominees of each identified stakeholder group (government officials, animal welfare representatives, animal scientists, stockpersons, producers/pre-export depot operators, exporters/ship owners and veterinarians), 18 potential indicators were identified Three levels were assigned to each using industry statistics and expert opinion, representing those observed on the best and worst 5% of voyages and an intermediate value. A computer-based questionnaire was completed by 135 stakeholders (48% of those invited). All indicators were ranked by respondents in the assigned order, except fodder intake, in which case providing the amount necessary to maintain bodyweight was rated better than over or underfeeding, and time in the pre-export assembly depot, in which case 5 days was rated better than 0 or 10 days. The respective Importance Values (a relative rating given by the respondent) for each indicator were, in order of declining importance: mortality (8.6%), clinical disease incidence (8.2%), respiration rate (6.8%), space allowance (6.2%), ammonia levels (6.1%), weight change (6.0%), wet bulb temperature (6.0%), time in assembly depot (5.4%), percentage of animals in hospital pen (5.4%), fodder intake (5.2%), stress-related metabolites (5.0%), percentage of feeding trough utilised (5.0%), injuries (4.8%), percentage of animals able to access food troughs at any one time (4.8%), percentage of animals lying down (4.7%), cortisol concentration (4.5Y.), noise (3.9y.), and photoperiod (3.4%). The different stakeholder groups were relatively consistent in their ranking of the indicators, with all groups nominating the some top two and at least five of the top seven indicators. Some of the top indicators, in particular mortality, disease incidence and temperature, are already recorded in the Australian industry, but the study identified potential new welfare indicators for exported livestock, such as space allowance and ammonia concentration, which could be used to improve welfare standards if validated by scientific data. The top indicators would also be useful worldwide for countries engaging in long distance sea transport of livestock.

Sorghum ergot can develop without local Claviceps africana inoculum from nearby infected plants

Batches of glasshouse-grown flowering sorghum plants were placed in circular plots for 24 h at two field sites in southeast Queensland, Australia on 38 occasions in 2003 and 2004, to trap aerial inoculum of Claviceps africana. Plants were located 20-200 m from the centre of the plots. Batches of sorghum plants with secondary conidia of C. africana on inoculated spikelets were placed at the centre of each plot on some dates as a local point source of inoculum. Plants exposed to field inoculum were returned to a glasshouse, incubated at near-100% relative humidity for 48 h and then at ambient relative humidity for another week before counting infected spikelets to estimate pathogen dispersal. Three times as many spikelets became infected when inoculum was present within 200 m of trap plants, but infected spikelets did not decline with increasing distance from local source within the 200 m. Spikelets also became infected on all 10 dates when plants were exposed without a local source of infected plants, indicating that infection can occur from conidia surviving in the atmosphere. In 2005, when trap plants were placed at 14 locations along a 280 km route, infected spikelets diminished with increasing distance from sorghum paddocks and infection was sporadic for distances over 1 km. Multiple regression analysis showed significant influence of moisture related weather variables on inoculum dispersal. Results suggest that sanitation measures can help reduce ergot severity at the local level, but sustainable management will require better understanding of long-distance dispersal of C. africana inoculum.

Cassowary dispersal of the invasive pond apple in a tropical rainforest: the contribution of subordinate dispersal modes in invasion.

Dispersal is a significant determinant of the pattern and process of invasions; however, weed dispersal distances are rarely described and descriptions of dispersal kernels are completely lacking for vertebrate-dispersed weeds. Here, we describe dispersal kernels generated by a native disperser, the endangered southern cassowary (Casuarius casuarius, L.) for an invasive, tropical rainforest plant, pond apple (Annona glabra, L.). Pond apple is primarily water-dispersed and is managed as such. We consider whether cassowary dispersal, as a numerically subordinate dispersal mode, provides an additional dispersal service that may modify the invasion process. In infested areas, pond apple seed was common in cassowary dung. Gut passage had no effect on the probability of single seed germination but deposition in clumps or as whole fruits reduced the probability of germination below that of single seeds. Gut passage times ranged from 65 to 1675 min. Combined with cassowary movement data, this resulted in estimated dispersal distances of 12.5-5212 m, with a median distance of 387 m (quartile range 112-787 m). Native frugivores can be effective dispersers of weeds in rainforest and even terrestrial dispersers can provide long-distance dispersal. Importantly, though pond apple might be expected to be almost entirely dispersed downstream and along the margins of aquatic and marine habitats, cassowaries provide dispersal upstream and between drainages, leading to novel dispersal outcomes. Even through the provision of small quantities of novel dispersal outcomes, subordinate dispersal modes can play a significant role in determining invasion pattern and influence the ultimate success of control programs by providing dispersal to locations unattainable via the primary mode.

Reproductive Biology of Corymbia citriodora subsp. variegata and Effective Pollination across its Native Range.

The spotted gum species complex represents a group of four eucalypt hardwood taxa that have a native range that spans the east coast of Australia, with a morphological cline from Victoria to northern Queensland. Of this group, Corymbia citriodora subsp. variegata (CCV) is widespread in south-eastern Queensland and northern New South Wales. It is currently the most commonly harvested native hardwood in Queensland. However, little basic knowledge of the reproductive biology of the species is available to inform genetic improvement and resource management programmes. Here we take an integrative approach, using both field and molecular data, to identify ecological factors important to mating patterns in native populations of CCV. Field observation of pollinator visitation and flowering phenology of 20 trees showed that foraging behaviour of pollinator guilds varies depending on flowering phenology and canopy structure. A positive effect of tree mean flowering effort was found on insect visitation, while bat visitation was predicted by tree height and by the number of trees simultaneously bearing flowers. Moreover, introduced honeybees were observed frequently, performing 73% of detected flower visits. Conversely, nectar-feeding birds and mammals were observed sporadically with lorikeets and honeyeaters each contributing to 11% of visits. Fruit bats, represented solely by the grey-headed flying fox, performed less than 2% of visits. Genotyping at six microsatellite markers in 301 seeds from 17 families sampled from four of Queensland's native forests showed that CCV displays a mixed-mating system that is mostly outcrossing (tm = 0.899 ± 0.021). Preferential effective pollination from near-neighbours was detected by means of maximum-likelihood paternity analysis with up to 16% of reproduction events resulting from selfing. Forty to 48% of fertilising pollen was also carried from longer distance (>60 m). Marked differences in foraging behaviour and visitation frequency between observed pollinator guilds suggests that the observed dichotomy of effective pollen movement in spotted gums may be due to frequent visit from introduced honeybees favouring geitonogamy and sporadic visits from honeyeaters and fruit bats resulting in potential long-distance pollinations.

Beyond fecundity control: which weeds are most containable?

1. Eradication is often the preferred strategy in the management of new weed invasions, but recent research has shown that the circumstances under which eradication can be achieved are highly constrained. Containment is a component of an eradication strategy and also a management objective in its own right. Just as for eradication, containment of a weed invasion should be attempted only if it is considered feasible. However, very little guidance exists for the assessment of containment feasibility for weeds. 2. Numerous factors have been proposed as influencing feasibility of containment, but those that relate to the potential for management of dispersal pathways and timely detection of new foci of infestation appear to be critical. Theory suggests that the rate of spread is largely driven by long-distance dispersal (LDD). However, LDD is generally unpredictable and often occurs for species that do not appear to be adapted for it. Furthermore, many (if not most) LDD events fail to give rise to new infestations. 3. As the probability of colonisation is related to the numbers of propagules immigrating ('propagule pressure') at a point in the landscape, dispersal pathways that move relatively large numbers of propagules simultaneously and/or repeatedly should most enhance weed spread. It is these pathways whose potential for management has the greatest bearing upon containment feasibility. A key impediment to containment is undetected spread; this need not occur through LDD and is more likely to occur through dispersal to lesser distances. 4. Synthesis and applications. Feasibility of containment should be viewed in terms of the effort required to reduce weed spread rate, as well as the effectiveness of relevant management actions. Where dispersal vectors are not readily manageable and the probability of detection via structured and/or unstructured surveillance is low, a much greater reliance upon fecundity control will be needed to contain a weed. A combination of empirical and theoretical approaches should be used to develop and refine estimates of containment feasibility. Such estimates will aid decision-making with regard to whether to attempt to reduce weed spread and assist in prioritisation of different weeds for containment.

Strangers in a strange land: do life history traits differ for alien and native colonisers of novel environments?

Do alien invasive species exhibit life history characteristics that are similar to those of native species that have become pests in their continent of origin? We compared eucalypt specialists that have become pests in Australian plantations (natives) to those that have established overseas (aliens) using 13 life history traits and found that although traits that support rapid population build-up were shared, overall, aliens and native colonisers differed significantly. Distance from source (New Zealand vs. other) had no significant effect, but species that established more than 50 years ago exhibited different life history traits from those that established within the last 50 years, possibly because of more effective quarantine. Native and alien eucalypt insect invaders differed predominantly in traits that facilitate long-distance movement (pathway traits), compared to traits that facilitate establishment and spread. Aliens had longer adult flight seasons, were smaller and more closely host-associated (cryptic eggs and larvae), had lower incidence of diapause (i.e. were more seasonally plastic) and more generations per year than natives. Thus, studies of species invasive within their country of origin can shed light on alien invasions.

Gene flow from Corymbia hybrids in northern New South Wales

Some of the most productive taxa for forestry are interspecific F1 hybrids grown as exotics in the tropics and subtropics. Attributes of resilience, adaptability and vigour which engender the hybrids for wood production, may also exacerbate the risk they present from gene flow to native species gene pools or to local ecologies as weeds. To determine the biological and genetic factors that influence the extent of hybridisation, we examine the distribution and genealogy of wildlings surrounding plantings of locally-exotic Corymbia torelliana (Section Cadageria) near native C. henryi (Section Maculatae) in northern New South Wales. Our study showed pre-mating and pre- and post-zygotic barriers were incomplete, with in situ generation and natural establishment of both F1 hybrids (n = 3) and advanced generation hybrids under the disturbed conditions bordering native forest. As hybrids were located on alluvial flats exposed to frost, they also likely have an extended ecological range relative to native C. henryi. Despite the likely generation of large viable seed crops on F1 trees at the site over many years, establishment success and survival of advanced generation hybrids may be low, as only 5 immature and no mature advanced generation hybrids were identified. Propagation and genetic analysis of a seed crop from one F1 wildling showed early survival and vigour of seedlings in cultivation was high, and that at least for some F1 in some seasons, backcrossing to the recurrent native C. henryi parent is favoured (60%), whereas selfing (10%) and crossing with other F1 (30%) was less frequent. Transport of seed by stingless bees probably accounted for long distance dispersal from C. torelliana, but this mechanism does not appear to supplement gravity-dispersal of seed from the F1. Coupled with other evidence from studies of bee behaviour, controlled pollination in Corymbia sp., and long-term fitness in second generation eucalypt hybrids, we anticipate gene flow via pollen rather than seed will be the greater challenge for managing the risk of introgression of C. torelliana ancestry into native species from the planted F1 hybrid. If large sources of F1 pollen become available to compete with native pollen, gene flow will probably be frequent and hybrids may establish in disturbed conditions and in habitats beyond the ecological range of their native parent. Further study is needed to determine the degree to which outbreeding depression and poor survival inhibits on-going gene flow.

Strangers in a strange land: do life history traits differ for alien and native colonisers of novel environments?

Do alien invasive species exhibit life history characteristics that are similar to those of native species that have become pests in their continent of origin? We compared eucalypt specialists that have become pests in Australian plantations (natives) to those that have established overseas (aliens) using 13 life history traits and found that although traits that support rapid population build-up were shared, overall, aliens and native colonisers differed significantly. Distance from source (New Zealand vs. other) had no significant effect, but species that established more than 50 years ago exhibited different life history traits from those that established within the last 50 years, possibly because of more effective quarantine. Native and alien eucalypt insect invaders differed predominantly in traits that facilitate long-distance movement (pathway traits), compared to traits that facilitate establishment and spread. Aliens had longer adult flight seasons, were smaller and more closely host-associated (cryptic eggs and larvae), had lower incidence of diapause (i.e. were more seasonally plastic) and more generations per year than natives. Thus, studies of species invasive within their country of origin can shed light on alien invasions.

Resilience of a eucalypt forest woody understorey to long-term (34–55 years) repeated burning in subtropical Australia

We investigated the effects of annual burning since 1952, triennial burning since 1973, fire exclusion since 1946 and infrequent wildfire (one fire in 61 years) on woody understorey vegetation in a dry sclerophyll eucalypt forest, south-eastern Queensland, Australia. We determined the influence of these treatments, and other site variables (rainfall, understorey density, topsoil C : N ratio, tree basal area, distance to watercourse and burn coverage) on plant taxa density, richness and composition. The richness of woody understorey taxa 0–1 m in height was not affected by burning treatments, but richness of woody plants 1–7.5 m in height was lower in the annually burnt treatment than in the triennially burnt treatment from 1989 to 2007. Fire frequency and other site variables explained 34% of the variation in taxa composition (three taxon groups and 10 species), of which 33% of the explained variance was explained by fire treatment and 46% was explained by other site variables. Annual burning between 1974 and 1993 was associated with lower understorey densities mainly due to reduced densities of eucalypts 1–7.5 m in height. Triennial burning during the same period was associated with higher densities of eucalypts 0–7.5 m in height relative to the annually burnt and unburnt treatments. Most woody taxa persisted in the frequently burnt treatments through resprouting mechanisms (e.g. lignotuberous regeneration), and fire patchiness associated with low-intensity burning was also found to be important. Persistence of plants <1 m tall demonstrates the resilience of woody taxa to repeated burning in this ecosystem, although they mainly exist in a suppressed growth state under annual burning.