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.

Resin-foraging by colonies of Trigona sapiens and T. hockingsi (Hymenoptera: Apidae, Meliponini) and consequent seed dispersal of Corymbia torelliana (Myrtaceae).

Resins are a critical resource for stingless bees and resin-collecting bees act as seed dispersers in tropical plants. We describe the diurnal foraging patterns of colonies of Trigona sapiens and T. hockingsi on resin and pollen. We also document patterns of waste removal and seed dispersal of Corymbia torelliana. At most, only 10% of foragers collected resin or dispersed seed. Nevertheless, bees dispersed 1-3 seeds outside the nest per 5 minutes, and 38-114 seeds per day for each nest. The proportion of returning bees carrying pollen was highest in the morning for both species. The proportion of foragers returning with resin loads showed no significant diurnal variation in any season. Waste removal activity peaked in the afternoon for T. sapiens and in the morning for T. hockingsi. Seed removal peaked in the afternoon in one year only for T. sapiens. Bees dispersed thousands of seeds of C. torelliana over the season even though only a small proportion of the colony was engaged in seed transport.

Ocean dispersal modelling for propagules of pond apple (Annona glabra L.)

Pond apple invades riparian and coastal environments with water acting as the main vector for dispersal. As seeds float and can reach the ocean, a seed tracking model driven by near surface ocean currents was used to develop maps of potential seed dispersal. Seeds were ‘released’ in the model from sites near the mouths of major North Queensland rivers. Most seeds reach land within three months of release, settling predominately on windward-facing locations. During calm and monsoonal conditions, seeds were generally swept in a southerly direction, however movement turns northward during south easterly trade winds. Seeds released in February from the Johnstone River were capable of being moved anywhere from 100 km north to 150 km south depending on prevailing conditions. Although wind driven currents are the primary mechanism influencing seed dispersal, tidal currents, the East Australian Current, and other factors such as coastline orientation, release location and time also play an important role in determining dispersal patterns. In extreme events such as tropical cyclone Justin in 1997, north east coast rivers could potentially transport seed over 1300 km to the Torres Strait, Papua New Guinea and beyond.

Contagious dispersal of seeds of synchronously fruiting species beneath invasive and native fleshy-fruited trees

In subtropical Australia, many native and invasive plant species rely on a shared suite of frugivores, largely birds, for seed dispersal. Many native plants fruit during summer in this region, whereas most invasive plants fruit during winter, thus providing the opportunity for contagious dispersal of seeds beneath synchronously fruiting species. We sampled invasive and native seed rain beneath the canopy of a native summer-fruiting tree Guioa semiglauca and an invasive winter-fruiting tree Cinnamomum camphora, in three study sites over the course of a year. In July, during peak fruiting season for C. camphora and other invasive species, seed rain of invasive species was higher beneath C. camphora than G. semiglauca. This was partly due to the invasive tree Ligustrum lucidum, whose seed rain was three times higher beneath C. camphora than beneath the native tree. In February, seed rain of native species was more abundant beneath the canopy of G. semiglauca than beneath C. camphora, despite the fact that C. camphora was also fruiting at this time. This was probably due to the larger fruit crop produced by G. semiglauca at this time of year. Our study provides evidence that the presence of invasive bird-dispersed plants may facilitate contagious seed dispersal of other invaders, and likewise native species may facilitate seed spread of other native plants.

Demographics, pollination syndrome and conservation status of Macrozamia platyrhachis (Zamiaceae), a geographically restricted Queensland cycad

To assess the International Union for Conservation of Nature (IUCN) status of Macrozamia platyrhachis F.M.Bailey, we surveyed this central Queensland cycad for its population abundance and health and its pollinator type and pollination syndrome (thermogenesis and volatile emissions). Plants are locally abundant within the 11 discrete populations surveyed, with an estimated population of 611 315 adult plants. Plants are highly restricted to a small area of occupancy, seed dispersal is nearly non-existent and extreme fires appear to have destroyed almost all seeds and seedlings and decimated the pollinators. Of known Macrozamia pollinators, only the thrips, Cycadothrips chadwicki Mound, were found on cones, and these were found in very low numbers. The pollination syndrome for this cycad appears to be unique, based on two cone traits. For one, thermogenesis peaks in early evening, a contrast with daytime peaks of other Cycadothrips-pollinated Macrozamia, but matches that of the Tranes weevil-pollinated Macrozamia machinii. In addition, cone volatiles include both previously unreported compounds as well as those reported exclusively on either Cycadothrips- or Tranes-pollinated species. Based on its small, fragmented area of occupancy, projected population declines and the unique pollination syndrome, we recommend that M. platyrhachis retain its current status as 'Endangered'. Habitat management plans should stipulate that controlled burns be avoided during cycad coning season and that wildfires be controlled to minimise damage to seedlings and pollinators.

Management of plant invasions mediated by frugivore interactions

1. Some of the most damaging invasive plants are dispersed by frugivores and this is an area of emerging importance in weed management. It highlights the need for practical information on how frugivores affect weed population dynamics and spread, how frugivore populations are affected by weeds and what management recommendations are available. 2. Fruit traits influence frugivore choice. Fruit size, the presence of an inedible peel, defensive chemistry, crop size and phenology may all be useful traits for consideration in screening and eradication programmes. By considering the effect of these traits on the probability, quality and quantity of seed dispersal, it may be possible to rank invasive species by their desirability to frugivores. Fruit traits can also be manipulated with biocontrol agents. 3. Functional groups of frugivores can be assembled according to broad species groupings, and further refined according to size, gape size, pre- and post-ingestion processing techniques and movement patterns, to predict dispersal and establishment patterns for plant introductions. 4. Landscape fragmentation can increase frugivore dispersal of invasives, as many invasive plants and dispersers readily use disturbed matrix environments and fragment edges. Dispersal to particular landscape features, such as perches and edges, can be manipulated to function as seed sinks if control measures are concentrated in these areas. 5. Where invasive plants comprise part of the diet of native frugivores, there may be a conservation conflict between control of the invasive and maintaining populations of the native frugivore, especially where other threats such as habitat destruction have reduced populations of native fruit species. 6. Synthesis and applications. Development of functional groups of frugivore-dispersed invasive plants and dispersers will enable us to develop predictions for novel dispersal interactions at both population and community scales. Increasingly sophisticated mechanistic seed dispersal models combined with spatially explicit simulations show much promise for providing weed managers with the information they need to develop strategies for surveying, eradicating and managing plant invasions. Possible conservation conflicts mean that understanding the nature of the invasive plant-frugivore interaction is essential for determining appropriate management.

Selecting replacements for invasive plants to support frugivores in highly modified sites: a case study focusing on Lantana camara

Invasive plants are regarded as a major threat to biodiversity worldwide. Yet, in some cases, invasive plants now perform important ecological functions. For example, fleshy-fruited invasive plants provide food that supports indigenous frugivore populations. How can the disparate goals of conservation versus invasive weed control be managed? We suggest using the fruit characteristics of the invasive plant to select replacement indigenous plants that are functionally similar from the perspective of frugivores. These could provide replacement food resources at sites where plants with these characteristics are part of the goal plant community and where such plants would not otherwise regenerate. Replacement plants could also redirect seed dispersal processes to favour indigenous, rather than invasive, plant species. We investigated the utility of this approach by ranking all indigenous fleshy-fruited plant species from a region using a simple model that scored species based upon measures of fruit phenology, morphology, conspicuousness and accessibility relative to a target invasive species, Lantana (Lantana camara). The model successfully produced high scores for indigenous plant species that were used by more of the frugivores of Lantana than a random selection of plants, suggesting that this approach warrants further investigation.

Comparative seed and dispersal ecology of three exotic subtropical Asparagus species

The genus Asparagus includes at least six invasive species in Australia. Asparagus aethiopicus and A. africanus are invasive in subtropical Australia, and a third species, A. virgatus is naturalized and demonstrates localized spread in south east Queensland. To better understand how the attributes of these species contribute to their invasiveness, we compared fruit and seed traits, germination, seedling emergence, seed survival, and time-to-maturity. We further investigated dispersal ecology of A. africanus, examining the diet of a local frugivore, the figbird (Sphecotheres viridis) and the effect of gut passage on seedling emergence. Overall, A. aethiopicus was superior in germination and emergence, with the highest mean germination (98.8%) and emergence (94.5%) under optimal conditions and higher emergence (mean of 73.3%) across all treatments. In contrast, A. africanus had the lowest germination under optimal conditions (71.7%) and low mean seedling emergence (49.5%), but had fruits with the highest relative yield (ratio of dry pulp to fruit fresh weight) that were favored by a local frugivore. Figbirds consumed large numbers of A. africanus fruits (~30% of all non-Ficus fruits), and seedling germination was not significantly affected by gut passage compared to unprocessed fruits. Asparagus virgatus germinated poorly under cool, light conditions (1.4%) despite a high optimum mean (95.0%) and had low mean performance across emergence treatments (36.3%). The species also had fruits with a low pulp return for frugivores. For all species, seed survival declined rapidly in the first 12 mo and fell to < 3.2% viability at 36 mo. On the basis of the traits considered, A. virgatus is unlikely to have the invasive potential of its congeners. Uniformly short seed survival times suggest that weed managers do not have to contend with a substantial persistent soil-stored seed bank, but frugivore-mediated dispersal beyond existing infestations will present a considerable management challenge.

Predicting dispersal and recruitment of Miconia calvescens (Melastomataceae) in Australian tropical rainforests

Miconia calvescens (Melastomataceae) is a serious invader in the tropical Pacific, including the Hawaiian and Tahitian Islands, and currently poses a major threat to native biodiversity in the Wet Tropics of Australia. The species is fleshy-fruited, small-seeded and shade tolerant, and thus has the potential to be dispersed widely and recruit in relatively intact rainforest habitats, displacing native species. Understanding and predicting the rate of spread is critical for the design and implementation of effective management actions. We used an individual-based model incorporating a dispersal function derived from dispersal curves for similar berry-fruited native species, and life-history parameters of fecundity and mortality to predict the spatial structure of a Miconia population after a 30 year time period. We compared the modelled population spatial structure to that of an actual infestation in the rainforests of north Queensland. Our goal was to assess how well the model predicts actual dispersion and to identify potential barriers and conduits to seed movement and seedling establishment. The model overpredicts overall population size and the spatial extent of the actual infestation, predicting individuals to occur at a maximum 1,750 m from the source compared with the maximum distance of any detected individual in the actual infestation of 1,191 m. We identify several characteristic features of managed invasive populations that make comparisons between modelled outcomes and actual infestations difficult. Our results suggest that the model’s ability to predict both spatial structure and spread of the population will be improved by incorporating a spatially explicit element, with dispersal and recruitment probabilities that reflect the relative suitability of different parts of the landscape for these processes.

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.

Variation in exotic and native seed arrival and recruitment of bird dispersed species in subtropical forest restoration and regrowth

Invasive bird-dispersed plants often share the same suite of dispersers as co-occurring native species, resulting in a complex management issue. Integrated management strategies could incorporate manipulation of dispersal or establishment processes. To improve our understanding of these processes, we quantified seed rain, recruit and seed bank density, and species richness for bird-dispersed invasive and native species in three early successional subtropical habitats in eastern Australia: tree regrowth, shrub regrowth and native restoration plantings. We investigated the effects of environmental factors (leaf area index (LAI), distance to edge, herbaceous ground cover and distance to nearest neighbour) on seed rain, seed bank and recruit abundance. Propagule availability was not always a good predictor of recruitment. For instance, although native tree seed rain density was similar, and species richness was higher, in native plantings, compared with tree regrowth, recruit density and species richness were lower. Native plantings also received lower densities of invasive tree seed rain than did tree regrowth habitats, but supported a similar density of invasive tree recruits. Invasive shrub seed rain was recorded in highest densities in shrub regrowth sites, but recruit density was similar between habitats. We discuss the role of microsite characteristics in influencing post-dispersal processes and recruit composition, and suggest ways of manipulating these processes as part of an integrated management strategy for bird-dispersed weeds in natural areas.

Seed persistence of the invasive aquatic plant, Gymnocoronis spilanthoides (Asteraceae)

Seed persistence of Gymnocoronis spilanthoides (D.Don) DC.; Asteraceae (Senegal tea), a serious weed of freshwater habitats, was examined in relation to burial status and different soil moisture regimes over a 3-year period. Seeds were found to be highly persistent, especially when buried. At the end of the experiment, 42.0%, 27.3% and 61.4% of buried seeds were viable following maintenance at field capacity, water logged and fluctuating (cycles of 1 week at field capacity followed by 3 weeks’ drying down) soil moisture conditions, respectively. Comparable viability values for surface-situated seeds were ~3% over all soil moisture regimes. Predicted times to1% viability are 16.2 years for buried seed and 3.8 years for surface-situated seed. Persistence was attributed primarily to the absence of light, a near-obligate requirement for germination in this species, although secondary dormancy was induced in some seeds. Previous work has demonstrated low fecundity in field populations of G. spilanthoides, which suggests that soil seed banks may not be particularly large. However, high levels of seed persistence, combined with ostensibly effective dispersal mechanisms, indicate that this weed may prove a difficult target for regional or state-wide eradication.

The need for speed: Timely prevention of the dispersal of noxious weeds in relief fodder using efficient sampling procedures

Invasive and noxious weeds are well known as a pervasive problem, imposing significant economic burdens on all areas of agriculture. Whilst there are multiple possible pathways of weed dispersal in this industry, of particular interest to this discussion is the unintended dispersal of weed seeds within fodder. During periods of drought or following natural disasters such as wild fire or flood, there arises the urgent need for 'relief' fodder to ensure survival and recovery of livestock. In emergency situations, relief fodder may be sourced from widely dispersed geographic regions, and some of these regions may be invaded by an extensive variety of weeds that are both exotic and detrimental to the intended destination for the fodder. Pasture hay is a common source of relief fodder and it typically consists of a mixture of grassy and broadleaf species that may include noxious weeds. When required urgently, pasture hay for relief fodder can be cut, baled, and transported over long distances in a short period of time, with little opportunity for prebaling inspection. It appears that, at the present time, there has been little effort towards rapid testing of bales, post-baling, for the presence of noxious weeds, as a measure to prevent dispersal of seeds. Published studies have relied on the analysis of relatively small numbers of bales, tested to destruction, in order to reveal seed species for identification and enumeration. The development of faster, more reliable, and non-destructive sampling methods is essential to increase the fodder industry's capacity to prevent the dispersal of noxious weeds to previously unaffected locales.

Seed bank longevity and age to reproductive maturity of Calotropis procera (Aiton) W.T. Aiton in the dry tropics of northern Queensland

Understanding the reproductive biology of Calotropis procera (Aiton) W.T. Aiton, an invasive weed of northern Australia, is critical for development of effective management strategies. Two experiments are reported on. In Experiment 1 seed longevity of C. procera seeds, exposed to different soil type (clay and river loam), pasture cover (present and absent) and burial depth (0, 2.5, 10 and 20 cm) treatments were examined. In Experiment 2 time to reach reproductive maturity was studied. The latter experiment included its sister species, C. gigantea (L.) W.T. Aiton, for comparison and two separate seed lots were tested in 2009 and 2012 to determine if exposure to different environmental conditions would influence persistence. Both seed lots demonstrated a rapid decline in viability over the first 3 months and declined to zero between 15 and 24 months after burial. In Experiment 1, longevity appeared to be most influenced by rainfall patterns and associated soil moisture, burial depth and soil type, but not the level of pasture cover. Experiment 2 showed that both C. procera and C. gigantea plants could flower once they had reached an average height of 85 cm. However, they differed significantly in terms of basal diameter at first flowering with C. gigantea significantly smaller (31 mm) than C. procera (45 mm). On average, C. gigantea flowered earlier (125 days vs 190 days) and set seed earlier (359 days vs 412 days) than C. procera. These results suggest that, under similar conditions to those that prevailed in the present studies, land managers could potentially achieve effective control of patches of C. procera in 2 years if they are able to kill all original plants and treat seedling regrowth frequently enough to prevent it reaching reproductive maturity. This suggested control strategy is based on the proviso that replenishment of the seed bank is not occurring from external sources (e.g. wind and water dispersal).

Dynamics of plant populations in Heteropogon contortus(black speargrass) pastures on a granite landscape in southern Queensland. 2. Seed production and soil seed banks of H. contortus

Seed production and soil seed hanks of H. contortus were studied in a subset of treatments within an extensive grazing study conducted in H. contortus pasture in southern Queensland between 1990 and 1996. Seed production of H. contortus in autumn ranged from 260 to 1800 seeds/m2 with much of this variation due to differences in rainfall between years. Seed production was generally higher in the silver-leaved ironbark than in the narrow-leaved ironbark land class and was also influenced by a consistent stocking rate x pasture type interaction. Inflorescence density was the main factor contributing to the variable seed production and was related to the rainfall received during February. The number of seeds per inflorescence was unaffected by seasonal rainfall, landscape position, stocking rate or legume oversowing. Seed viability was related to the rainfall received during March. Soil seed banks in spring varied from 130 to 520 seeds/m2 between 1990 and 1995 with generally more seed present in the silver-leaved ironbark than in the narrow-leaved ironbark land class. There were poor relationships between viable seed production and the size of the soil seed bank, and between the size of the soil seed bank and seedling recruitment. This study indicates that H. contortus has the potential to produce relatively large amounts of seed and showed that the seasonal pattern of rainfall plays a major role in achieving this potential