Invasional meltdown:  does invader-invader mutualism facilitate secondary invasions in rainforest on Christmas Island?

A project undertaken at the Department of Ecology, Environment & Evolution, La Trobe University by PhD student Luke O'Loughlin, and supervised by Dr Peter Green

Biological invasions are so pervasive that nearly all ecosystems contain many exotic species. One key consequence is that as the number of invasive species increase, they should increasingly interact not only with native species, but also with each other. Mutualistic interactions between successful ‘primary’ invaders can produce reciprocal, positive population-level effects that amplify their impacts, thereby altering properties of the recipient community to facilitate previous unsuccessful ‘secondary’ invaders. This process of ‘invasional meltdown’ adds a novel twist to the established theme in invasion biology that characteristics of the recipient community (such as biotic resistance and species diversity) are key determinants of invasion success.

The invasion of rainforest on Christmas Island by the exotic yellow crazy ant Anoplolepis gracilipes and a variety of introduced scale insect mutualists has long been considered the strongest evidence for invasional meltdown. The positive association between the ant and scale insects results in the formation of high-density ant supercolonies that accelerate and diversify impacts across rainforest on the Island. A key consequence of supercolony formation is the removal of the dominant omnivore-detritivore, the red land crab Gecarcoidea natalis. Occurring at naturally high densities, these crabs provide the recipient community with considerable biotic resistance against invaders in two ways. First, red crabs create high predation pressure on dispersing propagules that is consistent in both time and space. Second, by consuming and redistributing leaf litter, red crabs create spatial and temporal fluctuations in leaf litter cover and biomass, a challenging environment to the establishment of some invaders. However the yellow crazy ant, fuelled by carbohydrate from scale insects, causes local extinctions of red crabs, directly removing a major predator and indirectly increasing resources by deregulating seedling recruitment and leaf-litter breakdown, thereby creating a significantly different recipient community for prospective invaders.

One group of organisms on Christmas Island whose invasion success may be affected by the impacts yellow crazy ants and their scale insect mutualists are land snails. Thirty-eight species have been recorded from the Island, but 22 of these, including the Giant African Landsnail Achatina fulica (GALS) are not native to the island.  This project considered if the primary invaders (ants and scale insects) facilitated the invasion success of secondary invaders (exotic land snails) by eliminating red crabs and thereby altering key aspects of snail habitat – the creation of predator-free space, and alterations to leaf litter cover, biomass, and understory density. 

Surveys were conducted at 28 sites in four forest ‘states’ across the island; Intact forest supported the naturally high density of red crabs and where yellow crazy ants were never present (i.e. the reference condition), ii) Supercolonies were invaded by yellow crazy ants in high densities at the time of study, sufficient to extirpate the local red crab population, iii) Ghosted forest in which supercolonies had never formed, but in which red crabs were absent or rare because the local population had been killed while en route to the ocean during their annual breeding migration, and iv) Recovered forest where yellow crazy ant supercolonies had been removed through management action (baiting) and the area re-colonised by red crabs to a density similar to Intact forest.  Comparisons of abundance and composition between forest states showed that yellow crazy ants are not significant predators of land snails, the abundance of land snails is an order of magnitude higher were red crabs were absent, and that non-native species were present at all sites, including the control sites with naturally high densities of land crabs.  These results suggest quite strongly that yellow crazy ants, fuelled by their scale insect mutualists, facilitate invasion by permitting ‘population-release’ of exotic species.

Small-scale field experiments that manipulated red crab density and leaf litter biomass were conducted to determine whether the mechanism of invasion success was the creation of enemy-free space (relief from predation pressure) or the augmentation of habitat and resources. Small land snails (<2 mm long) were most abundant where resources where relatively high, regardless of the level of predation pressure.  However, large snails (> 2 mm long) were most abundant where predation pressure was low, regardless of the level of resources. These findings suggest a size-specific mechanism of invasion success; yellow crazy ants and scale insects  facilitate the invasion of large individuals (and species) by creating enemy-free space, but facilitate small individuals (and species) by indirectly augmenting habitat.

A number of approaches were undertaken to determine if there were impacts associated with the high abundance of one of these secondary invaders, the giant African land snail A. fulica. This pan-tropical invader is considered a significant agricultural pest, yet no study has assessed their impacts in a natural setting. An exclusion experiment found little to no evidence that highly abundant GALS has any impact on seedling recruitment or leaf litter dynamics. Direct observation and stable isotope analysis indicate GALS are primarily detritivorous, but the experiment showed that even at high density, these snails do not consume sufficient biomass to significantly lower the standing crop of litter.

Native biodiversity on Christmas Island is in crisis and our findings provide more evidence of the ‘invasional meltdown’ processes occurring in this impacted rainforest. This project has demonstrated that traits of the recipient community are critical to determining invasion success, and that the presence and impact of previously successful invaders should be considered among those traits.


O'Loughlin, LS and Green, PT (2015). Invader-invader mutualism influences land snail community composition and alters invasion success of alien species in tropical rainforest. Biol. Invasions 17, 2659-2674. DOI 10.1007/s10530-015-0903-6.

O'Loughlin, LS and Green, PT (2016). Habitat augmentation drives secondary invasion: an experimental approach to determine the mechanism of invasion success. Ecology 97(9), 2458-2469.

O'Loughlin, LS and Green, PT (2017). The secondary invasion of giant African land snail has little impact on litter or seedling dynamics in rainforest. Austral Ecology, 42, 819-830.

O'Loughlin, LS and Green, PT (2017). Secondary invasion: When invasion success is contingent on other invaders altering the properties of recipient ecosystems. Ecol Evol. 7, 7628-7637.

Figure Captions

Figure 1. The highly abundant omnivorous-detritivorous red land crab (Gecarcoidea natalis) dominates intact rainforest on Christmas Island. This keystone species keeps the forest floor free of leaf litter for much of the year and suppresses seedling recruitment. (Credit L. O’Loughlin)

Figure 2. By eliminating red crabs from large tracts of rainforest, yellow crazy ants, fuelled by honeydew-secreting scale insects, have significantly altered traits of the recipient community. The creation of enemy-free space and the release of habitat and resources were predicted to facilitate the secondary invasion of exotic land snails. (Credit L. O’Loughlin)

Figure 3.  Land snails of Christmas Island:

  1-3 Lamprocystis normani (E.A. Smith, 1888) Native
  4 Lamprocystis mabelae (E.A. Smith, 1888) Native
  5-7 Lamprocystis mildredae (E.A. Smith, 1888) Native
  8-9 Succinea solidula Pfeiffer, 1849 Introduced
  10-11 Succinea solitaria E.A. Smith, 1887 Native
  12-13 Succinea listeri E.A. Smith, 1888 Native
  14 Opeas pumilum (Pfeiffer, 1840) Introduced
  15 Pythia scarabaeus (Linné, 1758) Native
  16 Melampus luteus (Quoy & Gaimard, 1932) Introduced
  17 Melampus fasciatus (Deshayes, 1830) Introduced
  18 Melampus castaneus  (Mergle von Muhlfeld, 1816) Introduced
  19-20 Japonia wallacei (L. Pfeiffer, 1857) Native
  21-22 Truncatella guerinii  A. & J.B. Villa, 1841 Native
  23 Assiminea andrewsiana E.A. Smith, 1900 Native

(Credit Plate VIII in Andrews, CW (1900) A Monograph of Christmas Island (Indian Ocean). Published by the Trustees of British Museum (Natural History), London. (Wikimedia Commons)).

Figure 4. Subulina octona (Bruguière, 1792)  Introduced (Credit G. Neumann)

Figure 5. Paropeas achatinaceum (Pfeiffer, 1846)  Introduced (Credit G. Neumann)

Figure 6. Bradybaena similaris (Férussac, 1821)  Introduced (Credit G. Neumann)

Figure 7.  Achatina fulica Bowdich, 1822  Introduced (Credit Marshman at en.wikipedia / Eric Guinther - Transferred from en.wikipedia. Licensed under CC BY-SA 3.0 via Wikimedia Commons -

Figure 8. Red crab exclusion fences were erected in order to experimentally replicate a key trait of the recipient community created by the impacts of the invader-invader mutualism – low predation pressure.  The crabs were allowed to reduce leaf litter in some of these, but litter was added to others.  The snail fauna was sampled periodically on these exclosures.

Figure 9. The inverse of the experiment in Figure 8 was also done; red crabs were re-introduced to a site from which they had been absent, and the snail fauna was monitored. 

Figure 10.  Fences were erected to exclude the giant African land snail A. fulica from small test plots, to assess whether this highly abundant secondary invader has an impact on seedling and leaf litter dynamics. Land snails will not cross a copper surface so a simple fence with a copper-edged top is all that’s required.


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