1979; Formanowicz and Bradley, 1987; Inoue and Matsura, 1983; O’Brien
et al., 1990).Nematode–Insect Associations
Many nematode species have intimate heterospecific associations with
vertebrates, invertebrates and plants (i.e. symbiotic associations) (Cheng,
1991). Behavioural adaptations have probably played a critical role in
enabling nematodes to exploit this diversity of habitats (Croll, 1970;
Dusenberry, 1980). The symbiotic associations between nematodes and
insects are diverse and can be classified into three categories: phoretic
relationships, facultative parasitism and obligate parasitism (Poinar,
1975). Parasitic associations occur in many nematode families and are
likely to have evolved multiple times (Poinar, 1975; Blaxteret al., 1998).
Behavioural adaptations to increase the probability of encountering
insects were probably critical for facilitating this diversity of associations,
but our understanding of the behavioural interactions between nematodes
and insects is limited for most associations. The most thoroughly studied
species tend to be those with potential as biological control agents.
Phoresy is a phenomenon in which a life stage of one species is
transported by an animal of a different species (Farish and Axtell, 1971;
Houck and O’Connor, 1991). The degree of symbiosis in these phoretic
associations can vary considerably and transport can be external or inter-
nal. Phoresy may be the most common nematode–insect association, with
the phoretic life stage typically being a dauer juvenile (Massey, 1974;
Sudhaus, 1976; Kiontke, 1996). Phoresy is an important strategy for
species with limited mobility that exploit patchy and ephemeral
resources, such as rotting logs and animal waste. For example, the nema-
todeDiplogaster coprophilais a free-living species associated with animal
manure piles that produces a dauer juvenile phoretically associated with
some species of sepsid flies (Kiontke, 1996). Dauer juveniles aggregate on
fly pupae and initiate waving behaviour, which facilitates attachment to
emerging flies. Phoresy is likely to have been an important first step in the
evolution of many parasitic associations.
Nematodes that are facultative insect parasites can have free-living
generations, which are typically saprophagous. The degree of symbiosis
and harm caused to the host varies considerably among species (Poinar,
1972). A typical example of this type of association is Rhabditis
insectivora, which can complete its life cycle in the external environment
feeding on bacteria, but dauer juveniles that encounter larvae of
the cerambycid beetle,Dorcus parallelopipedus, enter the insect via the
digestive system and develop and mate in the haemocoel (Poinar, 1975).
Females leave the host to lay eggs, and only high rates of infection
are lethal to the insect. A more symbiotic facultative association occurs
between the nematodeDeladenus siricidicolaand the wood waspSirex
noctilio(Bedding, 1972, 1993). During free-living generations, which can16 J.F. Campbell and E.E. Lewis