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Keywords:

  • above-ground biomass;
  • angiosperms;
  • herbivory;
  • nitrogen content;
  • vegetation structure

Introduction

  1. Top of page
  2. Introduction
  3. Increasing quality of plant leaves as food through time
  4. A role for Red Queen?
  5. Conclusion
  6. Acknowledgements
  7. References

Hairston et al. (1960) asked why plant biomass accumulates in sufficient amounts to form vegetation, rather than being closely cropped by leaf-eating herbivores. They suggested a top-down hypothesis: predators/parasites prevent herbivore populations from building up to carrying capacity. Currently, however, plants are considered to be of too low a nutritional quality to be suitable as food for animals (e.g. Hartley & Jones, 1997; Polis, 1999). Most plants are ignored by most foliovores and that is why vegetation forms. Thus contemporary dynamic global vegetation models (DGVMs) typically ignore herbivory as a determinant of above-ground biomass (AGB) and mainly focus on net primary productivity (NPP) (e.g. Beerling & Woodward, 2001). However, NPP and AGB are not always correlated and herbivory is not always negligible. For example, temperate forests often have higher biomass than tropical forests (Midgley, 2001), although it remains to be seen whether differences in herbivory will explain this. In Africa, which uniquely still has most of its Pleistocene fauna, large herbivores such as elephants (Laws, 1970; Dublin et al., 1990) can seriously reduce AGB below that expected from NPP. Generalist herbivores, such as goats (e.g. Hendriks et al., 1992) overgraze many natural pastoral lands in Africa (e.g. Hoffman, 1997). This should not occur if plants are of too low a nutrient quality to be eaten.

Nevertheless, for many areas of Africa and elsewhere on the globe, abiotic or top-down factors are apparently more important in determining vegetation structure and AGB than are bottom-down factors such as herbivory. Plants appear to be ahead of foliovores in the evolutionary arms race and vegetation develops. Because forests date back to the Carboniferous, it appears that plants have always been ahead and vegetation has developed.

Besides nutrient quality, other factors also contribute to the reasons why plants are not totally consumed (e.g. Hartley & Jones, 1997; Polis, 1999). Secondary and other chemicals effectively lower food quality further, as do mechanical defences by increasing feeding time. The high patchiness of vegetation mosaics, high environmental variation (such as annual variation and interannual variation in climate), the vast numbers of plant species present, trophic structures and the impact of plant phenology/seasonality also limit herbivore reduction of AGB. Amongst nutrients, levels of protein (which largely corresponds to leaf nitrogen concentration, [N]) are seen as especially crucial (White, 1993; Polis, 1999).

Increasing quality of plant leaves as food through time

  1. Top of page
  2. Introduction
  3. Increasing quality of plant leaves as food through time
  4. A role for Red Queen?
  5. Conclusion
  6. Acknowledgements
  7. References

I argue that [N] in leaves in contemporary angiosperms is the highest it has ever been. Therefore leaf [N] can not presently be absolutely limiting because herbivory existed before angiosperms proliferated. For example, leaf-feeding arthropods existed in the late Carboniferous (Chaloner et al., 1991) and suites of herbivorous dinosaurs, including gigantic sauroprods, are well known from the Jurassic (e.g. Bakker, 1986).

The prediction that [N] in contemporary angiosperm leaves is likely to be the highest ever is possible because it is well known that [N] levels correlate strongly and positively with hydraulic capacities of plant species; the photosynthetic assimilation rate Amax correlates strongly with [N] and with rates of stomatal conductance (e.g. Wright et al., 2004). High rates of conductance require efficient hydraulic systems which are capable of delivering water at fast rates and of surviving cavitations during periods of stress. Thus the high levels of [N] in contemporary angiosperms, when compared with contemporary gymnosperms, cycads and ferns (e.g. Midgley et al., 2002), have only been possible because the evolution of xylem vessels is largely an angiosperm invention. Therefore, compared with leaf nutrient status of present angiosperms, the dominant plants of previous geological periods such as the Jurassic, when cycads, conifers and seed ferns dominated (e.g. Willis & McElwain, 2002), were probably of a lower nutrient concentration. Gymnosperms are also well known for high levels of secondary chemicals and possession of sclerophyllous small leaves – these are attributes which further limit their food quality.

Not only did nonangiosperm plants have photosynthetic organs of inherently low rates of photosynthesis, but higher levels of CO2 in previous times would have also acted to lower leaf [N] levels further per mouthful. For example, Beerling & Woodward (2001) argued that Palaeozoic plants must have had exceptionally low Rubisco (= leaf [N]) levels to explain the relative lack of fractionation of 13C noted in leaves from these periods, given their low stomatal densities and high ambient CO2 levels of that period. Recently, Korner (2004) summarised CO2 enrichment studies by concluding that higher CO2 levels tend to result in depleted leaf [N]. From the perspective of a foliovore, I suggest that high CO2 levels in previous epochs would have resulted in a lowering of forage quality per mouthful or bite.

Angiosperms appeared to have increased in abundance geologically in parallel with declining CO2 levels, whereas other groups such as gymnosperms have declined with declining CO2 levels (e.g. Willis & McElwain, 2002). Whether this is an explanation or correlation, the point is that in previous times, with both high CO2 levels and nonangiosperm plants, leaf quality must have been lower than it is at present, yet these periods supported the full range of foliovores. Present leaf quality is therefore not an absolute limit for it being considered as food for animal – it is a relative limit. Presumably, ancient nonmammalian foliovores would find contemporary angiosperms highly palatable.

A role for Red Queen?

  1. Top of page
  2. Introduction
  3. Increasing quality of plant leaves as food through time
  4. A role for Red Queen?
  5. Conclusion
  6. Acknowledgements
  7. References

I suggest the Red Queen Hypothesis (evolving to stay in the same relative place) explains in part why the world has vegetation despite the contemporary predominance of relatively nutrient-rich angiosperm leaves. This is because herbivore nutritional requirements will evolve in concert with food quality. Thus areas or epochs with food of lower relative quality will favour herbivores with relatively lower food quality requirements. As an example, Grubb (1992) noted the anomalous occurrence of extreme leaf spinescence in many Australian plants despite the low leaf [N] of these plants growing in this nutrient-poor continent. Again, low-nutrient plants should not be suitable food for herbivores and thus should not have experienced persistent significant vertebrate herbivory to have caused the evolution of antivertebrate herbivore defences such as spines. Grubb (1992) hypothesised that significant herbivory pressure was exerted by endemic Australian marsupials: their lower metabolical rates, when compared to eutherian mammals, would have allowed the former access to a relatively lower-quality diet. Marsupials also have ruminant-like fore-stomachs and an ability to recycle urinary nitrogen. The point is that herbivorous animals can deal with relatively low-quality food by the evolution of larger size, slower metabolisms/activity schedules and more efficient digestion and feeding behaviour.

The evolution of relatively higher-quality food in leaves as a consequence of the evolution of the angiosperms (nutritious ‘seeds’ are not an angiosperm invention) may have facilitated the spread of mammal foliovores with relatively higher metabolic rates. In part, the reason why we have vegetation then becomes the question of what caused the major evolutionary transitions between foliovore guilds. Possibly the evolution of angiosperms led to the competitive displacement of nonmammalian herbivores with lower metabolic rates.

Conclusion

  1. Top of page
  2. Introduction
  3. Increasing quality of plant leaves as food through time
  4. A role for Red Queen?
  5. Conclusion
  6. Acknowledgements
  7. References

I have argued that low food quality per se is not an absolute barrier to plants being considered as food. It is a relative barrier that depends on herbivore physiology, size, feeding habits and activity schedule/behaviour. Even wood, possibly the lowest-quality plant product, is considered as food (i.e. energy to fund N fixation) by some organisms in some places (e.g. Martin, 1991). The reason vegetation develops is because the forage nutrient requirements of foliovores evolves, leaving most plant species as being relatively unpalatable to most animal species.

Acknowledgements

  1. Top of page
  2. Introduction
  3. Increasing quality of plant leaves as food through time
  4. A role for Red Queen?
  5. Conclusion
  6. Acknowledgements
  7. References

I thank Peter Grubb, Andrew Illius, William Bond, Ian Woodward, David Coomes, Norman Owen-Smith, Nicci Illing and referees for useful comments.

References

  1. Top of page
  2. Introduction
  3. Increasing quality of plant leaves as food through time
  4. A role for Red Queen?
  5. Conclusion
  6. Acknowledgements
  7. References
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