Invasional meltdown: invader-invader mutualism facilitates a secondary invasion.

In multiply invaded ecosystems, introduced species should interact with each other as well as with native species. Invader-invader interactions may affect the success of further invaders by altering attributes of recipient communities and propagule pressure. The invasional meltdown hypothesis (IMH) posits that positive interactions among invaders initiate positive population-level feedback that intensifies impacts and promotes secondary invasions. IMH remains controversial: few studies show feedback between invaders that amplifies their effects, and none yet demonstrate facilitation of entry and spread of secondary invaders. Our results show that supercolonies of an alien ant, promoted by mutualism with introduced honeydew-secreting scale insects, permitted invasion by an exotic land snail on Christmas Island, Indian Ocean. Modeling of land snail spread over 750 sites across 135 km2 over seven years showed that the probability of land snail invasion was facilitated 253-fold in ant supercolonies but impeded in intact forest where predaceous native land crabs remained abundant. Land snail occurrence at neighboring sites, a measure of propagule pressure, also promoted land snail spread. Site comparisons and experiments revealed that ant supercolonies, by killing land crabs but not land snails, disrupted biotic resistance and provided enemy-free space. Predation pressure on land snails was lower (28.6%), survival 115 times longer, and abundance 20-fold greater in supercolonies than in intact forest. Whole-ecosystem suppression of supercolonies reversed the probability of land snail invasion by allowing recolonization of land crabs; land snails were much less likely (0.79%) to invade sites where supercolonies were suppressed than where they remained intact. Our results provide strong empirical evidence for IMH by demonstrating that mutualism between invaders reconfigures key interactions in the recipient community. This facilitates entry of secondary invaders and elevates propagule pressure, propagating their spread at the whole-ecosystem level. We show that identification and management of key facilitative interactions in invaded ecosystems can be used to reverse impacts and restore resistance to further invasions.

Genetic structure, behaviour and invasion history of the Argentine ant supercolony in Australia.

Biological invasions have significant ecological, evolutionary and economic consequences. Ants are exemplary invaders and their invasion success is frequently attributed to a shift in social structure between native and introduced populations. Here, we use a multidisciplinary approach to determine the social structure, origin and expansion of the invasive Argentine ant, Linepithema humile, in Australia by linking behavioural and genetic studies with indicators of dispersal pathways and propagule pressure. Behavioural assays revealed a complete absence of aggression within and between three cities - Melbourne, Adelaide and Perth - spanning 2700 km across Australia. Microsatellite analyses showed intracity genetic homogeneity and limited but significant intercity genetic differentiation. Exceptions were two Perth nests that likely represent independent translocations from Adelaide. These patterns suggest efficient local gene flow with more limited jump dispersal via transport corridors between cities. Microsatellite analyses of L. humile from potential source regions, combined with data from port interceptions, trade pathways and the timeline of spread within Australia, implicate the main European supercolony as the source of L. humile in Melbourne. Such an introduction probably then redistributed across Australia and spread to New Zealand to form an expansive Australasian supercolony.

Invasive ants disrupt frugivory by endemic island birds.

Biological invasions can alter direct and indirect interactions between species, generating far-reaching changes in ecological networks that affect key ecological functions. We used model and real fruit assays to show that the invasion and formation of high-density supercolonies by the yellow crazy ant (YCA), Anoplolepis gracilipes, disrupt frugivory by endemic birds on Christmas Island, Indian Ocean. The overall handling rates of model fruits by birds were 2.2-2.4-fold lower in ant-invaded than in uninvaded rainforest, and pecking rates by two bird species declined by 2.6- and 4.5-fold, respectively. YCAs directly interfered with frugivory; their experimental exclusion from fruiting displays increased fruit handling threefold to sixfold, compounding indirect effects of ant invasion on resources and habitat structure that influence bird abundances and behaviours. This invasive ant, whose high densities are sustained through mutualism with introduced scale insects, rapidly decreases fruit handling by endemic island birds and may erode a key ecological function, seed dispersal. Because most other invasive ant species form expansive, high-density supercolonies that depend in part on association with hemipteran mutualists, the effects that we report here on avian frugivore-plant associations may emerge across their introduced ranges.

Land crabs as key drivers in tropical coastal forest recruitment.

Plant populations are regulated by a diverse assortment of abiotic and biotic factors that influence seed dispersal and viability, and seedling establishment and growth at the microsite. Rarely does one animal guild exert as significant an influence on different plant assemblages as land crabs. We review three tropical coastal ecosystems-mangroves, island maritime forests, and mainland coastal terrestrial forests-where land crabs directly influence forest composition by limiting tree establishment and recruitment. Land crabs differentially prey on seeds, propagules and seedlings along nutrient, chemical and physical environmental gradients. In all of these ecosystems, but especially mangroves, abiotic gradients are well studied, strong and influence plant species distributions. However, we suggest that crab predation has primacy over many of these environmental factors by acting as the first limiting factor of tropical tree recruitment to drive the potential structural and compositional organisation of coastal forests. We show that the influence of crabs varies relative to tidal gradient, shoreline distance, canopy position, time, season, tree species and fruiting periodicity. Crabs also facilitate forest growth and development through such activities as excavation of burrows, creation of soil mounds, aeration of soils, removal of leaf litter into burrows and creation of carbon-rich soil microhabitats. For all three systems, land crabs influence the distribution, density and size-class structure of tree populations. Indeed, crabs are among the major drivers of tree recruitment in tropical coastal forest ecosystems, and their conservation should be included in management plans of these forests.

New mutualism for old: indirect disruption and direct facilitation of seed dispersal following Argentine ant invasion.

The indirect effects of biological invasions on native communities are poorly understood. Disruption of native ant communities following invasion by the Argentine ant (Linepithema humile) is widely reported to lead indirectly to the near complete collapse of seed dispersal services. In coastal scrub in southeastern Australia, we examined seed dispersal and handling of two native and two invasive alien plant species at Argentine ant-invaded or -uninvaded sites. The Argentine ant virtually eliminates the native keystone disperser Rhytidoponera victoriae, but seed dispersal did not collapse following invasion. Indeed, Argentine ants directly accounted for 92% of all ant-seed interactions and sustained overall seed dispersal rates. Nevertheless, dispersal quantity and quality among seed species differed between Argentine ant-invaded and -uninvaded sites. Argentine ants removed significantly fewer native Acacia retinodes seeds, but significantly more small seeds of invasive Polygala myrtifolia than did native ants at uninvaded sites. They also handled significantly more large seeds of A. sophorae, but rarely moved them >5 cm, instead recruiting en masse, consuming elaiosomes piecemeal and burying seeds in situ. In contrast, Argentine ants transported and interred P. myrtifolia seeds in their shallow nests. Experiments with artificial diaspores that varied in diaspore and elaiosome masses, but kept seed morphology and elaiosome quality constant, showed that removal by L. humile depended on the interaction of seed size and percentage elaiosome reward. Small diaspores were frequently taken, independent of high or low elaiosome reward, but large artificial diaspores with high reward instead elicited mass recruitment by Argentine ants and were rarely moved. Thus, Argentine ants appear to favour some diaspore types and reject others based largely on diaspore size and percentage reward. Such variability in response indirectly reduces native seed dispersal and can directly facilitate the spread of an invasive alien shrub.

Effects of an alien ant invasion on abundance, behavior, and reproductive success of endemic island birds.

Biological invaders can reconfigure ecological networks in communities, which changes community structure, composition, and ecosystem function. We investigated whether impacts caused by the introduced yellow crazy ant (Anoplolepis gracilipes), a pantropical invader rapidly expanding its range, extend to higher-order consumers by comparing counts, behaviors, and nesting success of endemic forest birds in ant-invaded and uninvaded rainforest on Christmas Island (Indian Ocean). Point counts and direct behavioral observations showed that ant invasion altered abundances and behaviors of the bird species we examined: the Island Thrush (Turdus poliocephalus erythropleurus), Emerald Dove (Chalcophaps indica natalis), and Christmas Island White-eye (Zosterops natalis). The thrush, which frequents the forest floor, altered its foraging and reproductive behaviors in ant-invaded forest, where nest-site location changed, and nest success and juvenile counts were lower. Counts of the dove, which forages exclusively on the forest floor, were 9-14 times lower in ant-invaded forest. In contrast, counts and foraging success of the white-eye, a generalist feeder in the understory and canopy, were higher in ant-invaded forest, where mutualism between the ant and honeydew-secreting scale insects increased the abundance of scale-insect prey. These complex outcomes involved the interplay of direct interference by ants and altered resource availability and habitat structure caused indirectly by ant invasion. Ecological meltdown, rapidly unleashed by ant invasion, extended to these endemic forest birds and may affect key ecosystem processes, including seed dispersal.

Recruitment dynamics in a rainforest seedling community: context-independent impact of a keystone consumer.

The influence of keystone consumers on community structure is frequently context-dependent; the same species plays a central organising role in some situations, but not others. On Christmas Island, in the Indian Ocean, a single species of omnivorous land crab, Gecarcoidea natalis, dominates the forest floor across intact rainforest. We hypothesised that this consumer plays a key role in regulating seedling recruitment and in controlling litter dynamics on the island, independent of the type of vegetation in which it occurred. To test this hypothesis, we conducted crab exclusion experiments in two forest types on the island and followed the dynamics of seedling recruitment and litter processing for six years. To determine if these effects were likely to be general across the island, we compared land crab densities and seedling abundance and diversity at ten sites across island rainforest. Surveys across island rainforest showed that seedlings of species susceptible to predation by land crabs are consistently rare. Abundance and diversity of these species were negatively correlated to red crab abundance. Although red land crabs may be important determinants of seedling recruitment to the overstorey, differences in overstorey and seedling composition at the sites suggests that recruitment of vulnerable trees still occurs at a temporal scale exceeding that of this study. These "windows" of recruitment may be related to infrequent events that reduce the effects of land crabs. Our results suggest that unlike the context dependence of most keystone consumers in continental systems, a single consumer, the red land crab, consistently controls the dynamics of seedling recruitment across this island rainforest.

Monopolization of litter processing by a dominant land crab on a tropical oceanic island.

Litter processing by macroinvertebrates typically involves suites of species that act together to determine rates of breakdown and decomposition. However, tropical oceanic islands and coastal fringes on continents are often dominated by one or a few species of omnivorous land crabs that consume leaf litter. We used an exclusion experiment, together with other leaf removal and litter decomposition studies, to assess the role of a single dominant species, the red crab (Gecarcoidea natalis), in litter dynamics in rain forest on Christmas Island, Indian Ocean. In the presence of red crabs, litter cover and biomass varied seasonally, from almost complete cover and high biomass at the end of the dry season to almost total absence of litter at the end of each wet season. When crabs were excluded from both the shaded understory and light gaps in rain forest, litter increased rapidly to almost complete cover, which was then maintained year round. Leaf tether experiments, and measures of litter input and standing crops, indicated that red crabs monopolize litter processing, removing between 39 and 87% of the annual leaf fall from the forest floor. Rates of litter turnover were over twice as high in the presence of land crabs: the decomposition constant, k, was 2.6 in the understory exclusion plots, but rose to 6.0 in the presence of crabs. Red crabs occur at biomass densities (114 g m-2) far greater than those reported elsewhere for entire litter faunas. They significantly reduced the abundance of other litter invertebrates, but we did not detect any change in the relative frequencies of the major invertebrate groups (mites, collembolans, pulmonate snails, ants, psocopterans, and spiders). Wherever omnivorous land crabs are abundant, their activities may be paramount in litter decomposition and in regulating the rate of nutrient cycling. In monopolizing litter processing, they may also be important physical "ecosystem engineers", translocating organic matter and nutrients into the soil and reducing available habitat for other animals.

Plants, mites and mutualism: leaf domatia and the abundance and reproduction of mites on Viburnum tinus (Caprifoliaceae).

Associations between mites and leaf domatia have been widely reported, but little is known about their consequences for either plants or mites. By excising domatia from leaves of the laureltinus, Viburnum tinus L. (Caprifoliaceae), in the garden and laboratory, we showed that domatia alter the abundance, distribution, and reproduction of potential plant mutualists. Over 4 months, leaves with domatia on six garden shrubs had 2-36 times more predatory and microbivorous mites, and more mite eggs than leaves without domatia. However, this effect varied among plants and was weaker on one shrub with few mites on its leaves. Domatia also influenced the distribution of mites on leaves. A significantly higher fraction of mites, representing all life stages, was found in vein axils of leaves with domatia than in vein axils on leaves without domatia. Single-leaf experiments in the laboratory showed that domatia enhanced reproduction by the predatory mite, Metaseiulus occidentalis, especially at low relative humidity (30-38%). When domatia were removed, oviposition was reduced significantly only at low relative humidity, suggesting that domatia provide mites with refuge from environmental extremes on the leaf surface. Moreover, the use of domatia by predatory mites may reduce the impact of some plant enemies. In two experiments where prey consumption was measured, M. occidentalis ate significantly higher percentages of the eggs of the two-spotted spider mite (Tetranychus urticae). Our results are consistent with the viewpoint that mite-domatia associations are mutualistic. By directly aiding and abetting the third trophic level, plants with leaf domatia may increase the efficiency of some predaceous and microbivorous mites in consuming plant enemies.

Seed dispersal by ants: behaviour-releasing compounds in elaiosomes.

In a study of the biochemical basis of seed dispersal by ants, elaiosomes of Acacia myrtifolia and Tetratheca stenocarpa induced seed collection: intact diaspores and elaiosomes were taken rapidly by ants while most seeds remained on the forest floor. Extracts of elaiosomes (non-polar lipids, polar lipids, and aqueous fractions) were differentially collected by ants. Small pieces of pith impregnated with the polar lipid fraction from elaiosomes of either species elicited a removal rate by ants equivalent to that of intact elaiosomes and significantly higher than that of untreated pith. The non-polar lipid fraction, highest in concentration in elaiosomes of both species, elicited removal that did not differ from that of untreated pith. In T. stenocarpa, however, the aqueous fraction also induced removal equivalent to the polar lipid fraction. 1,2-Diglycerides with unsaturated groups are present in the active polar fractions of both species and unsaturated oleate is the major acid group of the glycerides in elaiosomes. Most oleate-containing compounds tested were taken more rapidly by ants than saturated compounds, and oleic acid, associated with corpse-carrying in ants, induced rapid removal. 1,2-Diolein, but not 1,3-diolein, was taken suggesting that the specific configuration of fatty acid moieties influences collection by ants. We hypothesize that a small suite of oleyl-containing compounds in elaiosomes elicit a stereotyped carrying response by a variety of ants. While the nutrient composition of elaiosomes may provide the underlying selective advantage for ants in seed dispersal, specific compounds may manipulate their behaviour and maximize seed dispersal.

The effect of nutrients and inflorescence damage by insects on fruit-set by Banksia spinulosa.

We examined the role of added macronutrients (N, P, and K) and prevention of damage to inflorescences (ovule/seed predation and rachis damage) by insects in determining levels of fruit-set in Banksia spinulosa at two sites in southeastern Australia. Insecticide application eliminated damage to developing inflorescences (primarily by the lepidopteran, Arotrophora canthelias) and application of macronutrient fertilizer significantly increased nutrient concentrations in leaves at both sites. Only joint application of nutrients and insecticide increased fruit-set per infructescence significantly above that of the control, indicating that the effect of nutrients on fruit-set depends on the intensity of insect damage to inflorescences. The proportion of inflorescences that developed fruits differed between sites and higher levels of rachis damage at one site may partially explain the lower proportion of inflorescences that fruited. Neither nutrient addition or inflorescence damage influenced the position of fruit-set within an infructescence. Our results suggest that (1) macronutrient availability and inflorescence damage interact in determining levels of fruitset in B. spinulosa, and (2) other factors, such as pollen or micronutrient availability, may limit it at some sites. These results highlight site-specific variation and interaction in the factors that limit plant reproduction.

Ants and extrafloral nectaries: no evidence for plant protection in Helichrysum spp. - ant interactions.

Characterstics of Australian endemic Helichrysum bracteratum and H. viscosum suggest that foraging ants act as "guards" of developing flowerheads, protecting capitula from seed predators: (1) extrafloral nectar is secreted from leaves subtending the capitula and from bracts encircling the floral disc during pre- to post-flowering periods; (2) capitula are attended by ants; and, (3) encounters between ants and other capitula visitors, including predispersal seed predators such as Tephritis sp. (Diptera), can be frequent. In experiments to test the ant-guard hypothesis, exclusion of ants from plants increased abundance of other insects on the developing capitula. The difference between ant-access and ant-exclusion treatments was related to ant abundance on the access plants. These effects were statistically significant in spite of the large variation in insect activity between sites and through the season.The increased abundance of insects on capitula following ant-exclusion did not, however, result in significant increases in the number of adult seed predators observed on capitula, the number of immature seed predators in capitula, or capitula damage as estimated between ant-access and exclusion treatments of either H. bracteatum or H. viscosum. Further, the ant-exclusion treatment on H. bracteatum had no significant influence on pollination as measured by seed set or on the degree of parasitism of Tephritis sp. by Megastigmus sp. Site and season most strongly affected numbers of immature seed predators and damage to capitula.We discuss these findings in relation to the ant-guard hypothesis and suggest that generalization of the protection hypothesis to all plants with extrafloral nectaries is premature.

Foliar nectar production and ant activity on a neotropical tree, Ochroma pyramidale.

In second growth forest in lowland Costa Rica, ants forage at the foliar nectaries of juvenile Ochroma pyramidale. The relationship between leaf development, foliar nectar production and ant visitation indicates that nectar secretion and ant maintenance are greatest following rapid leaf expansion. Nectar measurements in the glasshouse corroborate field measurements showing that nectar production on a sapling is continuous through time and correlated with distribution and abundance of ants within a sapling. The presence of two nectary types, leaf vein and petiolar, on the leaves of O. pyramidale results in the continual maintenance of ants on the leaf undersurface. Nectar production of a sapling increases with increasing leaf area resulting in greater number of ants per sapling. Energetic costs of nectar production and ant maintenance appear low, representing about one per cent of the total energy invested in leaves.Spatial and diurnal patterns of ant activity changed very little over the study period. Removal and exclusion of ants from saplings results in the utilization of foliar nectar by trigonid bees. A significant difference in leaf damage between ant-visited and unvisited saplings, coupled with ant behavioral characteristics, is consistent with the hypothesis that ants act as antiherbivore agents on Ochroma.