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Plant–animal interactions: An evolutionary approach

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  2. Plant–animal interactions: An evolutionary approach

Ed. by C. M. Herrera & O. Pellmyr. 313 pages. Oxford UK: Blackwell Science Publishing, 2002. £35.00 s/b. ISBN 0-632-05267-8

Plant–animal interactions: an evolutionary approach is remarkable in that it successfully encompasses the effects of plant–animal interactions on both individuals and the wider ecosystem, and how such interactions were moulded by evolution. In exploring this, a comprehensive range of subject matter is used to explore the ancient, modern and usually complex relationships between plants and animals. The high degree of specialisation involved in these associations is demonstrated by examples of biological control methodologies, some of which have been unsuccessful because of an unexpected third party interaction.

The book opens with a diagrammatic representation of the major events in evolution, which is both detailed and clear. This effectively places palaeobiology in context. We are shown that plant characteristics are central to many aspects of natural history, especially trophic levels and food webs. Plants determine which herbivores are present, and this in turn determines which carnivores can survive in that habitat. The concepts of phylogeny and coevolution are introduced and clearly illustrated with examples from around the world. Floral biology and pollination strategies are possibly the easiest systems to accept as models for coevolution and speciation – or is it just luck that some orchids produce both a floral mimic and the exact chemical used as a sexual attractant by its pollinator wasps? We are shown how the smell, colour and axis of symmetry of flowers interact to attract the desired pollinator – and here at least size really does matter! Particularly intriguing is the idea that flowers could even be involved in sound transmission by acting as acoustic guides for bats. Although much of floral biology is descriptive, the book looks to the future with a description of the potential of molecular genetics both to dissect out interactions (which may involve multiple species) and to test hypotheses relating to the basis of attraction.

Plant–animal interactions usually fall into one of three categories, protection, shelter or food, and it is the latter which is covered in most depth. Examinations of the fossil record and dinosaur stomach contents have revealed the origins of invertebrate and vertebrate herbivory. Fossil information indicates that food is the main reason for evolutionary change and that adaptations can be beneficial for considerable periods of evolutionary time. The 1origin of vertebrate herbivory is believed to be due largely to the evolution of specialised mouthparts which could dictate and drive what or how to eat. This is elegantly demonstrated by the variation in bat mouthparts according to food source. The importance of mouthpart evolution is corroborated by the statistics (just under one fifth of all terrestrial plant biomass is removed by herbivores) but it is explained that herbivore type is just as important in determining the final habitat makeup. Vertebrate herbivores have the potential to remove plant parts whole and so could have a greater impact on plant populations than invertebrate herbivores. In fact, grasslands can be considered to be an extreme example of this type of plant–animal interaction, as they are believed to have originated as a result of vertebrate herbivores developing specialised grinding teeth.

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Figure 1. Credit: Sitona lineatus on Pisum sativum. Courtesy of Serge Carré, INRA, France.

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With the onset of herbivory comes the need for the plants to protect themselves. As discussed early in the book, the fossil record reveals the ‘arms race’ between plants and animals to be an ancient phenomenon. Secondary metabolites are crucial to this interaction and have multiple roles in defence against pathogens/predators, protection of fruit until the seeds are ready for dispersal and conversely as attractants to pollinators or seed dispersal agents. This raises an interesting conundrum – how much effort should a plant invest in attraction vs defence for a given reward in fitness? The discussion of herbivore load and fitness of host and herbivore is touched on in several places. In the context of biochemical defences it is a pity that wounding responses in plants are not discussed as fully as other topics. A summary table of secondary compounds and potential signalling molecules would be well placed.

Trophic levels are inefficient in transfer of energy and so mutualisms have evolved to maximise efficiency of food use. For example, recruitment of microorganisms in the gut to aid with the digestion of lignin and cellulose is seen both in insects and in larger herbivores such as cattle and sheep with their specialised rumen. A comparison of digestive systems is presented from the simplest (human) to most complex (ruminant). This reflects the physiological limitations of food selection although the basis of choice is far more complex and the effects often surprising. Examples from both leaf and fruit feeders prove that digestive refinements together with habitat-based limitations contrive to push the boundaries of sustainable body size in relation to diet selection.

Considerations of food quality justifiably include nutrients and antinutrients. There is some very good background on the nutritive value of plants but what makes this account novel is that the variability of forage quality is discussed. It is clear that addressing forage quality on the basis of chemical composition alone is inadequate if an understanding of the relationship between those chemicals and the herbivore is lacking. It is pointed out that although, generally, nitrogen is the main determinant of food selection, this does depend on (a) herbivore species and (b) form of nitrogen used as a storage compound in a particular plant species. Seasonal effects make some plants unpalatable or even toxic at certain times, or there may be a reliance on feeding stimuli of which the researcher is unaware. This goes some way to answering the question of why food selection on the basis of apparent quality (chemical composition) may be inconsistent.

Plant–animal interactions can have far reaching consequences for the environment and so any attempts to gain a more complete understanding of such relationships are timely. The way that the size and type of seed determines the interactions with dispersal agents and hence the distribution radius (Janzen-Cornell model) is covered in some detail in more than one place in this book. Herbivory may also involve predation of seeds (granivory). The specialised reward body (elaiosome) attached to the seed in ant-dispersed seeds and the positive selection pressure exerted on seed production by herbivory are just two of the examples given to demonstrate strategies that plants use in either preventing or accepting seed predation. Perhaps less obvious is the conclusion that granivory can actually promote species diversity via imperfect hoarding practices or disturbance of the seedbank, and this can be effected by classes of animals from rodents to ants. There is also a detailed explanation as to how herbivory can affect nutrient cycling, which then has a direct effect on the timing and availability of nutrients to plants and so affects the succession of colonising plant species. The ensuing species composition will in turn affect animal diversity via availability of housing and the establishment of new food webs. It is argued that in temperate grasslands plant–animal interactions not only maintain species diversity but also help to prevent tree invasion and maintain the traditional look of much of our countryside. These are important clues to best practice while western agriculture is attempting to become more environmentally benign.

This book encourages us all to consider complementary methodology in tackling complex biological problems. At the beginning of the book the case is put for the pivotal role of flight in the colonisation of land by both plants and animals. This should encourage us all to look beyond the boundaries of our own research area. Only through multidisciplinary biology do the complex relationships involved in species diversity of both plants and animals become unravelled. Maintaining species diversity is important because it promotes interactions which can have unusual follow-on effects. For example, the ability of some plants to accumulate toxic heavy metals may initially have been a defence against herbivores, but is now being exploited by man in reclamation of contaminated soils, which may eventually become diverse habitats. Many valid areas for future research are suggested: interspecific hybridisation, control of polyploidy, the marine ecosystem, the cause of patchiness in herbivory. Intrinsic to these is the recognition of the importance of long-term field ecology. These are challenging questions that need to be answered by careful observation and construction of detailed models. Furthermore, it is acknowledged that microbiology is currently under-represented in research into mutualisms even though bacteria and fungi play a key role in many interdependent systems (e.g. the complex interaction of plants, ants, their fungal gardens and the bacteria of the genus Streptomyces which protects against a pathogen of the fungus).

In general the text of this book is lively and generously illustrated. The authors are not afraid to challenge conventional assumptions, which are sometimes found wanting in the light of recent evidence. Possibly the only notable omission is a general glossary section (although there is some explanation of specialist terminology provided in Chapter 2, which would make some parts of the text more accessible to the reader lacking a background in evolutionary biology). The book is intended for use by undergraduates, but the detail of some chapters and relevance of some of the arguments may be more suited to those actively involved in research. In summary, I would recommend this book to anyone with an interest in natural history as well as students and researchers in the ecological and biological sciences.