Introduction symbionts mutualists commensals and engineers

No species lives in isolation, but often the association with another species is especially close: for many organisms, the habitat they occupy is an individual of another species. Parasites live within the body cavities or even the cells of their hosts; nitrogen-fixing bacteria live in nodules on the roots of leguminous plants; and so on. Symbiosis ('living together') is the term that has been coined for such close physical associations between species, in which a 'symbiont' occupies a habitat provided by a 'host'.

In fact, parasites are usually excluded from the category of sym-bionts, which is reserved instead for interactions where there is at least the suggestion of 'mutualism'. A mutualistic relationship is simply one in which organisms of different species interact to their mutual benefit. It usually involves the direct exchange of goods or services (e.g. food, defense or transport) and typically results in the acquisition of novel capabilities by at least one partner (Herre et al., 1999). Mutualism, therefore, need not involve close physical association: mutualists need not be symbionts. For example, many plants gain dispersal of their seeds by offering a reward to birds or mammals in the form of edible fleshy fruits, and many plants assure effective pollination by offering a resource of nectar in their flowers to visiting insects. These are mutualistic interactions but they are not symbioses.

It would be wrong, however, to see mutualistic interactions simply as conflict-free relationships from which nothing but good things flow for both partners. Rather, current evolutionary thinking views mutualisms as cases of reciprocal exploitation where, none the less, each partner is a net beneficiary (Herre & West, 1997).

Nor are interactions in which one species provides the habitat for another necessarily either mutualistic (both parties benefit:

'+ +') or parasitic (one gains, one suffers: '+ —'). In the first place, it may simply not be possible to establish, with solid data, that each of the participants either benefits or suffers. In addition, though, there are many 'interactions' between two species in which the first provides a habitat for the second, but there is no real suspicion that the first either benefits or suffers in any measurable way as a consequence. Trees, for example, provide habitats for the many species of birds, bats and climbing and scrambling animals that are absent from treeless environments. Lichens and mosses develop on tree trunks, and climbing plants such as ivy, vines and figs, though they root in the ground, use tree trunks as support to extend their foliage up into a forest canopy. Trees are therefore good examples of what have been called ecological or ecosystem 'engineers' (Jones et al., 1994). By their very presence, they create, modify or maintain habitats for others. In aquatic communities, the solid surfaces of larger organisms are even more important contributors to biodiversity. Seaweeds and kelps normally grow only where they can be anchored on rocks, but their fronds are colonized in turn by filamentous algae, by tube-forming worms (Spirorbis) and by modular animals such as hydroids and bryozoans that depend on seaweeds for anchorage and access to resources in the moving waters of the sea.

More generally, many of these are likely to be examples of commensal 'interactions' (one partner gains, the other is neither harmed nor benefits: '+ 0'). Certainly, those cases where the harm to the host of a 'parasite' or the benefit to a 'mutualist' cannot be established should be classified as commensal or 'host-guest', bearing in mind that, like guests under other circumstances, they may be unwelcome when the hosts are ill or distressed! Commensals have received far less study than parasites and mutualists, though many of them have ways of life that are quite as specialized and fascinating.

Mutualisms themselves have often been neglected in the past compared to other types of interaction, yet mutualists compose most of the world's biomass. Almost all the plants that dominate mutualism: reciprocal exploitation not a cosy partnership

Figure 13.1 (a) Cleaner fish really do clean their clients. The mean number of gnathiid parasites per client (Hemigymnus melapterus) at five reefs, from three of which (14, 15 and 16) the cleaners (Labroides dimidiatus) were experimentally removed. In a 'long-term' experiment, clients without cleaners had more parasites after 12 days (upper panel: F = 17.6, P = 0.02). In a 'short-term' experiment, clients without cleaners did not have significantly more parasites at dawn after 12 h (middle panel: F = 1.8, P = 0.21), presumably because cleaners do not feed at night, but the difference was significant after a further 12 h of daylight (lower panel: F = 11.6, P = 0.04). Bars represent standard errors. (After Grutter, 1999.) (b) Cleaners increase reef fish diversity. The percentage change in the number of fish species present following natural or experimental loss of a cleaner fish, L. dimidiatus, from a reef patch (or the two treatments combined), in the short term (2-4 weeks, light bars) and the long term (4-20 months, dark bars). (c) The percentage change in the number of fish species present following natural or experimental immigration of a cleaner fish, L. dimidiatus, into a reef patch (or the two treatments combined), in the short term (2-4 weeks, light bars) and the long term (4-20 months, dark bars). The columns and error bars represent medians and interquartiles. *, P < 0.05; **, P < 0.01; ***, P < 0.001. (After Bshary, 2003.)

(b) Cleaner gone

20 r

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