Can the fig-fig wasp pollination mutualism persist in a fragmented landscape?

A project undertaken at Ecosystem Management, The University of New England, and supervised by Caroline Gross

  • John Nason and Mary Harris, Department of Ecology, Evolution and Organisational Biology, Iowa State University;
  • Mohammed Fatemi, D, Mackay and C Stehn, Ecosystem Management , University of New England
  • Xiaohong Yao, Wuhan Botanic Gardens, China

This study was concerned with the impact of habitat fragmentation on the mutualism between the Australian endemic tree Ficus rubiginosa (Moraceae) and its fig wasp community, comprised of the pollinator (Pleistodontes imperialis, Agaonidae) and non-pollinating fig wasps (NPFWs). The work was undertaken in eastern Australia.

Habitat fragmentation is a key driver of biodiversity loss, and as a global phenomenon shows no sign of abating in the near future.  For many plant species, fragmentation not only has a demographic impact, through reduced abundance and distribution, but also results in the disruption of essential biotic associations, such as pollination and seed dispersal mutualisms. This has led some researchers to suggest that we are on the precipice of a co-extinction crisis due to the interdependent and entwined fates of many mutualistic pairs. What then can we learn about the impacts of habitat fragmentation from the highly specialised mutualism between host fig and pollinating fig wasp?    

The three hypotheses that we tested were;

  • H1: Within-tree asynchrony in flowering and inbreeding increases in small, spatially isolated populations;
  • H2: Increased within-tree asynchrony results in increased parasite and parasitoid loads;
  • H3: Habitat fragmentation decreases genetic diversity within and connectivity among fig populations. 

We worked in 24 populations, 12 of these intensively, and we harvested more than 2500 fruits from 483 trees over the three years of the study.  From these fruits we processed more than 59 000 wasps and 5000 seedlings for genotyping. We developed new microsatellite primers for Ficus rubiginosa which we used to describe the amount of inbreeding in populations.

We rejected all three hypotheses. We found no support that a harsh climate causes trees to rely upon selfing for reproductive assurance.  We found high levels of outbreeding and strong evidence that this is due to the hyper-dispersive behaviour of the pollinator wasps.  We did detect an influence of climate on pollinator abundance, and non-pollinating wasp abundance but this did not have a regulating effect on seed-set as trees out west produce less flowers (and seed) than in mesic east coast environments.

We found eight species of Agaonoid wasps in a trophic structure involving the ovule resource (which includes the pollinator Pleistodontes imperialis) and a further six species involved in trophic food web involving the fig wall tissue.

We show that the F. rubiginosa/P. imperialis mutualism to be remarkably resilient to the effects of a range of environmental and ecological variables.  Climatic variability appears to have the largest impact on the mutualistic partners through the effect it has on resource availability, which includes the common resource of female flowers.  Although this impact affects both partners in a similar way and consequently mutualism stability is maintained, albeit at a reduced rate of productivity. Non-pollinating fig wasps also had little observable impact on the mutualism, and once again variability in flower number is likely to be an important factor in determining the strength of this interaction.

We found very high levels of outbreeding in our seedling cohorts which was not influenced by habitat context (large population versus small, contiguous versus fragmented). 
We found little structuring of genetic diversity among populations when all of our populations were included in the analysis indicating that gene flow among populations overcomes the obstacles of fragmentation where connectivity of habitat has been disrupted by human activities (farming, mining) or by natural vicariance (disjunct rock outcrops).

The current study provides evidence that resource availability and climate are key drivers of reproductive output and mutualism stability within the F. rubiginosa - P. imperialis mutualism.  Syconia productivity was largely determined by environmental factors, of which rainfall and edaphic differences are likely to be the most important.  Flower number similarly increases along this gradient. These environmental factors appear to affect both mutualistic partners in a similar way, with the resource-poor inland sites having lower productivity but also a reduced rate of ovule exploitation by the pollinating wasp.  In the highly productive syconia of the coastal sites, pollinating wasp exploitation was at its highest, but seed production still increased. Variation in the rate of pollinating fig wasp exploitation across the longitudinal gradient may act to reduce conflict in the mutualism at sites towards the edge of the natural range of F. rubiginosa, potentially moderating the mutualism in these resource poor, dry western sites.

Figure Legends

Figure 1. The figs of Ficus rubiginosa. These ones are approaching D stage (when pollen is released from anthers and pollinators collect the pollen from the flowers before emerging from the fig, via a small hole pre drilled by a male wasp). Image C.L. Gross

Figure 2.  A female Pleistodontes imperialis wasp emerging from the fig. Image C.L. Gross

Figure 3.  A Philotrypesis female just emerged from a fig. We found 15 species of fig wasps in this study system. Image C. Stehn.

Figure 4. Ficus rubiginosa is an important food resource for many species of bird, including the Wompoo pigeon (Ptilinopus magnificus) in the Sawtell area. Image C.L. Gross

Figure 5. Collecting figs at the Boggabri site of Gins leap. Note the fragmented landscape. Image C.L. Gross

Figure 6. The Kaputar field site. Ficus rubiginosa grows along the cliff edges and in the ravines. Image C.L. Gross

Figure 7. At Dripping Rock, the fig trees cling to rock shelves and ledges. Image C.L. Gross

Figure 8. Fruit collecting in the sites. Fruits are measured in the field then cracked open before storing in a jar. Wasps emerge into the jars from the fruit. Image C.L. Gross



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