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The functional relationships between fish distribution and the selected predictors show similar nonlinear interactions across models (Figure 4). All models show dome shaped responses to prey availability, with fish selecting patches of high, but not maximum, zooplankton densities (Figure 4A). Physical samples revealed dominance of cladocerans Ceriodaphnia dubia, Bosmina longirostris and the copepod Boeckella gracilipes, key prey items for Galaxias maculatus during summer [9]. Average densities and zooplankton composition conformed to previous studies [9], [21], demonstrating pronounced spatial aggregation (Figure 5A), where fish feeding rates are likely limited by pursuit and handling time, rather than encounter rates within local prey patches. The functional relationships with predation risk, estimated as the proportion of large targets (>20 cm), corresponding to the size distribution of native prey vs. introduced predators (Figure S3), demonstrate an exponentially decaying function overall, with declining densities or probability of presence, as the predation risk increases (Figure 4B).
Apart from releasing more biocontrols and trying to chop out the plants where feasible, are there any other options available Perhaps inadvertent experiments have been performed by land managers which could provide insights into new ways of managing this alien woody scourge In densely invaded landscapes, patches of land are on occasion encountered which are mysteriously free of the alien woody invaders. Have these patches been cleared meticulously by land managers, or are there other forces at play Perhaps the soil conditions are not suitable for the germination of the woody plants' seeds, or there are specific seed predators present in the patches, but not in the surrounding landscape Or perhaps the plants in these patches are more competitive than the invading woody plant seedlings and prevent them from recruiting by smothering them above ground, strangling their roots below ground, releasing toxins in the soil that damage them, or taking up nutrients faster than them
Taking these questions into account, we searched for sites in and around the southwestern Cape Floristic Region where there were sizeable patches (at least several hectares) of non-invaded land within densely invaded landscapes. We found seven such sites where there were no plausible reasons for why alien woody plants had not invaded certain patches of land. Land use histories of the sites are provided in Table 1. Three of these tree-free patches (at the Blaauwberg, Rooshook and Vergelegen sites) were old agricultural lands, with mixes of herbaceous alien weeds, alien grasses and ruderal fynbos. The other four patches (at the Bothasig, Dassenberg, Klein Dassenberg and Joostenbergkloof sites) were in previously uncultivated vegetation i.e. intact fynbos. We analysed the chemistry of topsoils in the non-invaded patches and the surrounding invaded landscape.
Although it is feasible that certain soil physical or organic chemical properties had prevented germination of the alien woody plant seeds, or certain seed predators had consumed the seeds before they germinated at our study sites, we focused our research on soil inorganic nutrients, which we consider to be a more likely explanation for the constraint of the woody plants. In particular, we tested the explanatory power of what is known as the Catabolic Theory.10-12 This theory holds that short plants (namely herbs, grasses and shrubs) will outcompete tree seedlings when demand for catabolic nutrients (e.g. P, Cu and Zn) is met by supply - with this demand being partly dependent on the availability of anabolic nutrients (e.g. B, Mg and Mn).13-15 The reasoning underpinning the theory is that if a soil nutritional regime favours the production over the metabolism of photosynthates, then a photosynthate surplus arises, which will be used for synthesising wood. The concept of short plants outcompeting tree seedlings is not new16, and the Catabolic Theory has been corroborated by studies on treeless vegetation surrounded by treed vegetation in both Australia and South Africa14,15.
The results of our investigation support the Catabolic Theory. Although many nutrients are likely to be involved in the interplay between the short plants in the non-invaded patches and the alien woody invaders, two nutrients were particularly noteworthy: phosphorus (P) and boron (B). Old agricultural lands were consistently enriched in P, compared with the adjacent invaded landscapes (Figure 1). This observation suggests that an ample amount of P allows the ruderal herbaceous species to outcompete the alien woody plants. Moreover, in the case of B, all of the non-encroached sites, with the exception of Joostenbergkloof, had significantly lower concentrations of B than did the surrounding invaded landscape (Figure 2). This finding suggests that a scarcity of B favours fynbos plants over woody plant invaders.
Although soil amendments would be a radical approach to conserving fynbos, the current threat from woody alien invaders is so grave that all options need to be put on the table and carefully scrutinised, no matter how startling. Furthermore, new ideas and new experiments are needed to develop a deeper understanding of why the woody alien invaders are so pervasive in the first place. Without such an understanding, it is difficult to pioneer new options for management in a coherent, systematic manner. The simple explanations of a lack of natural predators20-22 and carbon dioxide fertilisation23,24 are surely just valuable chapters in a complex story. A long-term fertilisation experiment in a South African savanna has shown conclusively that changes in soil nutrient regimes can either promote or entirely constrain woody plant encroachment.15 It is highly probable that soil nutrients exert similar strong controls on woody plants in all biomes globally, not only in South African savannas. There are 13 plant nutrients which have the potential to affect the competitive interplay between fynbos plants and their woody alien invaders. It is high time that we started understanding these effects.
5. Gaertner M, Den Breeyen A, Hui C, Richardson DM. Impacts of alien plant invasions on species richness in Mediterranean-type ecosystems: A meta-analysis. Prog Phys Geogr. 2009;33(3):319-338. [ Links ]6. Van Wilgen BW, Fill JM, Baard J, Cheney C, Forsyth AT, Kraaij T. Historical costs and projected future scenarios for the management of invasive alien plants in protected areas in the Cape Floristic Region. Biol Conserv. 2016;200:168-177. [ Links ]7. Moran VC, Hoffmann JH. Conservation of the Fynbos biome in the Cape Floral Region: The role of biological control in the management of invasive alien trees. BioControl. 2012;57(2):139-149. -011-9403-5 [ Links ]8. Moran VC, Hoffmann JH, Zimmermann HG. Biological control of invasive alien plants in South Africa: Necessity, circumspection, and success. Front Ecol Environ. 2005;3:71-77. -9295(2005)003[0071:BCOIAP]2.0.CO;2 [ Links ]9. Rouget M, Richardson DM, Cowling RM, Lloyd JW, Lombard AT. Current patterns of habitat transformation and future threats to biodiversity in terrestrial ecosystems of the Cape Floristic Region, South Africa. Biol Conserv. 2003;112:63-85. -3207(02)00395-6 [ Links ]10. Milewski AV, Mills AJ. Does life consistently maximise energy intensity Biol Rev. 2010;85(4):859-879. -185X.2010.00131.x [ Links ]11. Milewski AV, Mills AJ. Why was the Highveld treeless Looking laterally to the Pampas for global edaphic principles beyond biogeographical accidents. S Afr J Bot. 2015;101:98-106. [ Links ]12. Mills AJ, Milewski AV, Rogers KH, Witkowski ETF, Stalmans M. Boundary of treeless grassland in relation to nutrient content of soils on the Highveld of South Africa. Geoderma. 2013;200:165-171. [ Links ]13. Mills AJ, Milewski AV, Fey MV, Gröngröft A, Petersen A, Sirami C. Constraint on woody cover in relation to nutrient content of soils in western southern Africa. Oikos. 2013;122(1):136-148. -0706.2012.20417.x [ Links ]14. Mills AJ, Milewski AV, Sirami C. A preliminary test of catabolic nutrients in explanation of the puzzling treelessness of grassland in mesic Australia. Austral Ecol. 2016;41(8):927-937. [ Links ]15. Mills AJ, Milewski AV, Snyman D, Jordaan JJ. Effects of anabolic and catabolic nutrients on woody plant encroachment after long-term experimental fertilization in a South African savanna. PLoS One. 2017;12(6), e0179848, 24 pages. [ Links ]16. Knoop AWT, Walker BH. Interactions of woody and herbaceous vegetation in a southern African savanna. J Ecol. 1985;73(1):235-253. [ Links ]17. Hingston FJ. Reactions between boron and clays. Soil Res. 1964;2(1):83-95. [ Links ]18. Keren R, Mezuman U. Boron adsorption by clay minerals using a phenomenological equation. Clays Clay Miner. 1981;29(3):198-204. [ Links ]19. Kim Y, Kirkpatrick RJ. 11B NMR investigation of boron interaction with mineral surfaces: Results for boehmite, silica gel and illite. Geochim Cosmochim Acta. 2006;70(13):3231-3238. [ Links ]20. Andersen AN. How important is seed predation to recruitment in stable populations of long-lived perennials Oecologia. 1989;81(3):310-315. [ Links ]21. Crawley MJ. Insect herbivores and plant population dynamics. Annu Rev Entomol. 1989;34(1):531-562. [ Links ]22. Maron JL, Vilà M. When do herbivores affect plant invasion Evidence for the natural enemies and biotic resistance hypotheses. Oikos. 2001;95(3):361-373. -0706.2001.950301.x [ Links ]23. Bradley BA, Blumenthal DM, Wilcove DS, Ziska LH. Predicting plant invasions in an era of global change. Trends Ecol Evol. 2010;25(5):310-318. [ Links ]24. Richardson DM, Bond WJ, Dean RJ, Higgins SI, Midgley GF, Milton SJ, et al. Invasive alien species and global change: A South African perspective. In: Mooney HA, Hobbs RJ, editors. Invasive species in a changing world. Washington DC: Island Press; 2000. p. 303-349. [ Links ] 153554b96e
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